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Possible Hybridization Between the Peruvian Booby Sula Variegata and the Blue-footed Booby S Nebouxii in Lobos De Afuera Islands, Peru

Authors:
Judith Figueroa at Asociación para la Investigación y Conservación de la Biodiversidad, Perú
Judith Figueroa
  • Asociación para la Investigación y Conservación de la Biodiversidad, Perú
Marcelo Stucchi
Marcelo Stucchi
Marcelo Stucchi
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Abstract

In 2004, two aberrant boobies with coloration characteristics hared by the Blue-footed and Peruvian boobies were observed. As in Ayala (2006), the head of the aberrant booby was light brown, the eyes were bright orange and the legs were grey as in the Peruvian Booby. In contrast, the wing secondary feathers were brown, similar to those in the Blue-footed Booby, without the variegated pattern of the Peruvian Booby. In 2005, an aberrant booby was observed with the same characteristics as seen in the two other cases, except that the feet were light turquoise. In all cases, the aberrant boobies were adult males found in the Blue-footed Booby colony. Also, they were always seen courting Blue-footed Boobies with vocalizations very similar to those of the male of that species. Additionally, G. Macurí (pers. comm. 2004) observed, in September 2004 at a nest without eggs, a couple formed by a Peruvian Booby and a Blue-footed Booby.
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Figueroa & Stucchi: Possible hybridization of boobies in Lobos de Afuera Islands 75
Marine Ornithology 36: 75–76 (2008)
75
The Blue-footed Booby Sula nebouxii breeds in the California Gulf
(Mexico), the Panama Gulf (Panama) and on the Galapagos (Ecuador),
Lobos de Tierra and Lobos de Afuera islands (Peru) (Nelson 1978).
The Peruvian Booby S. variegata is a bird endemic to the Peruvian
Current and its breeding distribution follows the Peruvian coast, from
Lobos de Tierra Island to Morro Sama (Peru) and to the central coast
of Chile (Nelson 1978). These species coincide geographically in the
islands of Lobos de Tierra and Lobos de Afuera; however, at both
islands, the populations of the Blue-footed Booby are much larger
(Ayala 2006, Stucchi & Figueroa 2006).
In November 2004 and August 2005, we visited the Lobos de
Afuera Islands (06°57′S, 80°41′W), which are 93 km west of
Lambayeque, Peru. The group is formed of several islets and rocks,
approximately 2.36 km2 in area. Four species of the Sulidae have
been reported in these islands: Blue-footed Booby, Peruvian Booby,
Nazca Booby S. granti and Masked Booby S. dactylatra (Figueroa
2004). The latter is a rare species; the Blue-footed and Peruvian
boobies are both very abundant (Stucchi & Figueroa 2006).
In 2004, two aberrant boobies with coloration characteristics hared
by the Blue-footed and Peruvian boobies were observed. As in
Ayala (2006), the head of the aberrant booby was light brown, the
eyes were bright orange and the legs were grey as in the Peruvian
Booby. In contrast, the wing secondary feathers were brown,
similar to those in the Blue-footed Booby, without the variegated
pattern of the Peruvian Booby (Fig. 1). In 2005, an aberrant booby
was observed with the same characteristics as seen in the two other
cases, except that the feet were light turquoise. In all cases, the
aberrant boobies were adult males found in the Blue-footed Booby
colony. Also, they were always seen courting Blue-footed Boobies
with vocalizations very similar to those of the male of that species.
Additionally, G. Macurí (pers. comm. 2004) observed, in September
2004 at a nest without eggs, a couple formed by a Peruvian Booby
and a Blue-footed Booby.
Nelson (1978) argues that hybridization may occur between the
Masked Booby and the Brown Booby S. leucogaster. Pitman &
Jehl (1998) found, in the Clipperton and San Benedicto islands,
individuals whose beaks had a coloration intermediate between
the Nazca Booby and the Masked Booby, which those authors
suggested may be some form of hybrid. In March 1999 on Lobos
de Tierra Island, JF observed courtship behaviour between a Blue-
footed Booby and a Nazca Booby, and in June that same year,
the presence of an aberrant booby, with the same characteristics
described by Ayala (2006). Pierotti (1987) found, in an analysis of
more than one hundred different seabird species, that whenever they
nest sympatrically, species with similar coloured beaks and feet are
more likely to hybridize.
Sulidae have been present on the Peruvian coast since the early
middle Miocene (Stucchi & DeVries 2003). During the late
Miocene and the Pliocene a radiation of up to seven species has been
identified (Stucchi 2003, Stucchi & Urbina 2004) among which
S. aff. variegata and four new species were reported. This radiation
is ecologically equivalent to the one found in North America,
where the genus Morus predominates (Warheit 2001), suggesting
an independent evolutionary history. Friesen & Anderson (1997)
suggest that the extant species appeared in no more than three
million years and that S. variegata and S. nebouxii have speciated
since the last interglacial period. The scarce interspecific variability
(in many cases, lower than intraspecific variability) of extant
and fossil Sulidae (Warheit 1992, Stucchi 2003) and the constant
hybridization of the species, reported in this work and by Ayala
(2006), could indicate that the parapatric speciation suggested by
Friesen and Anderson (1997) have permitted an open gene flow in
the last millions of years.
In conclusion, it appears that the evolution of Sulidae is more
complex than is suggested by molecular studies in extant species.
POSSIBLE HYBRIDIZATION BETWEEN THE PERUVIAN BOOBY
SULA VARIEGATA AND THE BLUE-FOOTED BOOBY S. NEBOUXII
IN LOBOS DE AFUERA ISLANDS, PERU
JUDITH FIGUEROA & MARCELO STUCCHI
AICB Asociación para la Investigación y Conservación de la Biodiversidad, Av. Vicús 538, Lima, 33, Perú
(aicb.peru@gmail.com)
Received 21 March 2007, accepted 14 February 2008
Fig. 1. An aberrant booby (left) and Blue-footed Booby Sula
nebouxii (right), Lobos de Afuera Islands, Peru, November 2004.
Photo by M. Stucchi.
76 Figueroa & Stucchi: Possible hybridization of boobies in Lobos de Afuera Islands
Marine Ornithology 36: 75–76 (2008)
ACkNOWLEDGEMENTS
To the Proabonos (guano extraction company) for the entry permit
to the islands and logistic support from Mariano Valverde, Pedro
Sotelo, Osmar Navarro, Walter Cano and Gustavo Macurí. To
the Dirección de Hidrografía de la Marina de Guerra del Perú
(Hydrography Department of the Peruvian Navy) for the use of
their facilities and transfer to the islands, especially Wanner Puicón,
Eduardo Mendoza, Oscar Marcoz, José Cholán, Dennis Huanca,
Jaime Gamboa, Abel Martínez and Felipe Portugal. To Ismael
Ignacio, José Yarlequé, Esteban Ezequiel, Gregorio García and the
crew of their boats, for their support in the transfer to the islands
and collaboration. To Idea Wild for the donation of field equipment.
We are grateful to Tatiana Cavero for her help in translating the
manuscript.
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Lobos de Afuera y algunos alcances sobre su biodiversidad.
Asociación Ucumari. Reporte de Investigación No 2. 88 pp.
WARHEIT, K. 1992. The role of morphometrics and cladistics
in the taxonomy of fossils: a paleornithological example.
Systematic Biology 41: 345–369.
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paleontology in understanding seabird community structure.
In: Schreiber, E.A. & Burger, J. (Eds). Biology of marine birds.
Boca Raton, FL: CRC Press. 17-55 pp.
... Blue-footed Sula nebouxii and Peruvian S. variegata boobies breed within the eastern tropical and subtropical Pacific Ocean, and both species are capable of long distance dispersal ( Fig. 1; Nelson 1978, Aid et al. 1985, Simeone et al. 2002. They are parapatric (Nelson 1978), hybridize on two islands, Lobos de Tierra and Lobos de Afuera in northern Peru (Ayala 2006, Figueroa and Stucchi 2008, Taylor et al. 2010b, and diverged recently (0.25-0.45 mya) Anderson 1997, Patterson et al. 2010). Blue-footed boobies outnumber Peruvian boobies on Lobos de Tierra by an order of magnitude (Zavalaga unpubl.), ...
... Aberrant individuals possessing characteristics intermediate between blue-footed and Peruvian boobies have been recorded on both islands where the species co-occur (Ayala 2006, Figueroa and Stucchi 2008, Taylor et al. 2010b. These intermediate individuals are commonly observed in breeding pairs, and have thus far been reported as females paired to male blue-footed boobies (Ayala 2006, Taylor et al. 2010b, or males courting female blue-footed boobies (Figueroa and Stucchi 2008). ...
... Aberrant individuals possessing characteristics intermediate between blue-footed and Peruvian boobies have been recorded on both islands where the species co-occur (Ayala 2006, Figueroa and Stucchi 2008, Taylor et al. 2010b. These intermediate individuals are commonly observed in breeding pairs, and have thus far been reported as females paired to male blue-footed boobies (Ayala 2006, Taylor et al. 2010b, or males courting female blue-footed boobies (Figueroa and Stucchi 2008). The majority of intermediate females were observed successfully laying eggs and raising chicks (Ayala 2006), or incubating eggs (Taylor et al. 2010b), indicating that backcrossing between these species occurs. ...
Evidence for strong assortative mating, limited gene flow, and strong differentiation across the blue-footed/Peruvian booby hybrid zone in northern Peru
Article
Full-text available
  • Jul 2012
Hybrid zones represent natural laboratories in which the processes of divergence and genetic isolation can be examined. The generation and maintenance of a hybrid zone requires mispairing and successful reproduction between organisms that differ in one or more heritable traits. Understanding the dynamics of hybridization between two species requires an understanding of the extent to which they have diverged genetically, the frequency of misparing and hybrid production, and the extent of introgression. Three hundred and twenty one blue-footed Sula nebouxii and Peruvian S. variegata boobies from the eastern tropical Pacific Ocean were analyzed using 19 putatively neutral genetic markers to evaluate interspecific differentiation, to classify morphological hybrids using Bayesian assignments, and to characterize hybridization using cline theory and Bayesian assignments. The species were well differentiated at mitochondrial and nuclear microsatellites, the hybrid zone was bimodal (contained a high frequency of each parental species but a low frequency of hybrids), and morphologically intermediate individuals were most likely F1 hybrids resulting from mating between female Peruvian boobies and male blue-footed boobies. Clines in allele frequency could be constrained to share a common geographic centre but could not be constrained to share a common width. Peruvian and blue-footed boobies hybridize infrequently, potentially due to strong premating reproductive isolation; however, backcrossing appears to facilitate introgression from blue-footed to Peruvian boobies in this hybrid system.
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... They exhibit weak (blue-footed boobies) [28] or no (Peruvian boobies) [29] intraspecific population structure at neutral loci. They are sister species that diverged recently (0.25-1.1 mya) [30,31], and that hybridize occasionally where their ranges overlap on two islands in northern Peru, Isla Lobos de Tierra and Isla Lobos de Afuera (Fig. 1) [30][31][32][33][34][35]. On Lobos de Tierra, blue-footed boobies outnumber Peruvian boobies by an order of magnitude and the species tend to form distinct colonies. ...
... On Lobos de Afuera, bluefooted and Peruvian boobies exist at relatively equal numbers, and overlapping breeding aggregations on this island are not uncommon (Taylor pers obs). Interspecific courting behaviour has been documented on both islands [32,33,35]; however, the level of hybridization that occurs in this system does not violate the modified biological species concept [36]. Both species have restricted distributions within the eastern Tropical Pacific, but have relatively large and stable populations [37]. ...
... The asymmetrical gene exchange we detected, from Peruvian to blue-footed boobies, is generally consistent with recorded contemporary hybridization ( Figure 4A) [32,33,34,35]. All contemporary hybrids reported in Taylor et al. (2012) possessed Peruvian booby mitochondrial DNA and the nuclear genotype of F1 hybrids, suggesting they were the product of hybridization between a female Peruvian booby and a male blue-footed booby ( Figure 4A). ...
Evidence for Asymmetrical Divergence-Gene Flow of Nuclear Loci, but Not Mitochondrial Loci, between Seabird Sister Species: Blue-Footed (Sula nebouxii) and Peruvian (S. variegata) Boobies
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Understanding the process of speciation requires understanding how gene flow influences divergence. Recent analyses indicate that divergence can take place despite gene flow and that the sex chromosomes can exhibit different levels of gene flow than autosomes and mitochondrial DNA. Using an eight marker dataset including autosomal, z-linked, and mitochondrial loci we tested the hypothesis that blue-footed (Sula nebouxii) and Peruvian (S. variegata) boobies diverged from their common ancestor with gene flow, paying specific attention to the differences in gene flow estimates from nuclear and mitochondrial markers. We found no gene flow at mitochondrial markers, but found evidence from the combined autosomal and z-linked dataset that blue-footed and Peruvian boobies experienced asymmetrical gene flow during or after their initial divergence, predominantly from Peruvian boobies into blue-footed boobies. This gene exchange may have occurred either sporadically between periods of allopatry, or regularly throughout the divergence process. Our results add to growing evidence that diverging species can remain distinct but exchange genes.
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... En la primavera de 2004, se estimó 35,000 individuos en las islas(Figueroa y Stucchi 2008a). En noviembre del mismo año, se observó en las islas Cachimbo e Independencia dos individuos híbridos entre el piquero peruano y el camanay(Figueroa y Stucchi 2008c). En febrero de 2011 se observó a la mayoría de los individuos con polluelos en su primer mes de edad(Figueroa y Stucchi 2012a). ...
Línea Base Biológica Terrestre y Marina de la Reserva Nacional Sistema de Islas, Islotes y Puntas Guaneras - Islas Lobos de Afuera. Capítulo 1: Caracterización de la fauna: aves, mamíferos y reptiles
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  • Dec 2019
Hasta el cierre del análisis de datos de la línea base biológica, en 2016, se obtuvo un total de 43 especies. Posteriormente, en 2017 y 2018, se registraron tres nuevas especies: garcita bueyera (Bubulcus ibis), gaviota de capucha gris (Chroicocephalus cirrocephalus) y playero pectoral (Calidris melanotos), haciendo un total de 46 especies para las islas Lobos de Afuera y el mar adyacente. Estas se encuentran agrupadas en diez órdenes y 20 familias. En relación a la información de la línea base biológica, la mayor parte de la avifauna estuvo representada por el orden Charadriiformes (gaviotas, chorlos y playeros) con el 32.56% de las especies, seguido de Procellariiformes (golondrinas de mar y petreles) con el 25.58% y Suliformes (piqueros y cormoranes) con el 20.93%. A nivel de familias, Laridae (gaviotas y gaviotines) estuvo representada por el 13.95% de las especies, seguida de Procellaridae, Sulidae y Scolopacidae con el 11.63%. Se reportó la reproducción de diez especies de aves en las islas. El guanay (Phalacrocorax bougainvillii) se reproduce de manera ocasional (1999, 2012, 2014 y 2016), mientras que las otras nueve especies se reproducen anualmente: pingüino de Humboldt (Spheniscus humboldti), camanay (Sula nebouxii), piquero peruano (Sula variegata), piquero de pico naranja o de Nazca (Sula granti), cushuri (Phalacrocorax brasilianus), pelícano peruano (Pelecanus thagus), gaviota peruana (Larus belcheri), gaviota dominicana (Larus dominicanus) y zarcillo (Larosterna inca). Sobre la base de los constantes registros del potoyunco peruano (Pelecanoides garnotii) y la golondrina de mar peruana (Oceanodroma tethys) en las islas, es probable que haya alguna pequeña colonia reproductiva en un área adyacente. Asimismo, 17 especies de aves (39.53%) fueron migratorias, de estas diez fueron emigrantes boreales (albatros de Galápagos, golondrina de mar negra, zarapito trinador, playero vagabundo, vuelvepiedras, faláropo de pico grueso, faláropo de pico delgado, salteador pomarino, gaviota tijereta y gaviota de Franklin) y siete australes (albatros de cabeza gris, petrel gigante sureño, petrel damero, petrel de mentón blanco, pardela gris, golondrina de mar chica y gaviota gris). Por otro lado, se registró cinco especies de mamíferos: lobo marino chusco (Otaria byronia), ballena jorobada (Megaptera novaeangliae), delfín común (Delphinus capensis), delfín nariz de botella (Tursiops truncatus), y uno introducido, la rata negra (Rattus rattus). Finalmente, sobre los reptiles se reportó a la lagartija (Microlophus peruvianus), el gecko (Phyllodactylus microphyllus) y la tortuga verde (Chelonia mydas).
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Hybridization from Possible Sexual Mis-imprinting: Molecular Characterization of Hybridization Between Brown Sula Leucogaster and Blue-footed Boobies S Nebouxii
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The Masked Booby Sula dactylatra has a wide distribution range, breeding on most tropical islands around the world (Nelson 1978, Pitman & Jehl 1998). In the eastern Pacific Ocean, Masked Boobies nest on Alijos and Revillagigedos (Mexico), Clipperton (France, off southwestern Mexico), Galapagos (Ecuador) and Juan Fernandez (Chile) islands. The recently described Nazca Booby S. granti has a smaller distribution range, breeding only on Revillagigedos, Clipperton, Malpelo (Colombia), Galapagos and La Plata (Ecuador) islands (Pitman & Jehl 1998, Fig. 1). The identification of these two similar-looking boobies is based on bill and leg colour. The Masked Booby has a yellow bill and light-olive-coloured legs; the Nazca Booby has an orange (male) or coral-red (female) bill and khaki-grey-coloured legs (Pitman & Jehl 1998, D.J. Anderson pers. comm.). Pitman & Jehl (1998) included the northern coast of Peru as the probable overlap area between Masked and Nazca Boobies. Jahncke & Goya (1997) reported the presence of breeding Masked Boobies on Lobos de Tierra Island (6°28′S, 80°50′W) in northern Peru. However, that report was published before the Nazca Booby was recognized as a full species (Pitman & Jehl 1998). The morphologic characteristics of the boobies found breeding on Lobos de Tierra Island are more similar to those of Nazca than of Masked Boobies (J. Jahncke pers. comm.). During late March 2000, I visited the Peruvian Lobos de Afuera Islands to assess the diversity of the sulid species present. The islands are located in an ecotone area, where cold water from the Peruvian Current meets warm water from the El Niño Current. Roberson (1998) mentioned that breeding sites of these species are related to this type of ecosystem. The Lobos de Afuera Islands (6°56′S, 80°42′W) are located 93 km off the coast from Lambayeque. The locality consists of two islands with a total area of 235 ha (Carbajal et al. 2001). During this investigation, four species of the genus Sula were observed. The previously reported Blue-footed Booby S. nebouxii (Tovar 1968) and Peruvian Booby S. variegata (Nelson 1978) were both observed incubating eggs. Masked and Nazca Boobies were also both observed on the island for the first time. I observed three adult Masked Boobies and nine Nazca Boobies (three incubating pairs, one pair attending an empty nest and a single adult). I did not find chicks or juveniles of either Masked or Nazca Boobies. Both species were found in the same general rocky area used by Blue-footed Boobies.
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In most species of birds, differences in plumage coloration or song structure act as isolating mechanisms. In seabirds, plumages are generally drab, and vocal repertoires are limited so that other phenotypic attributes must act as isolating mechanisms. One classic study of gulls suggests that the contrast between eye color and head color acts as a reproductive isolating mechanism, but this idea has been largely refuted by widespread evidence of hybridization in gulls in the last 20 years. An examination of more than 100 species of seabirds that breed sympatrically with congeners reveals that species with bills and feet similar in color hybridize in all areas where they breed sympatrically. Species that have bills or feet of different colors either do not hybridize or they produce rare hybrids that are unable to obtain mates as adults. This suggests that bill and foot coloration act as the primary isolating mechanisms in all surface-nesting seabirds and some burrow nesters. It may be a general pattern in birds that foot color acts to supplement bill color in reproductive isolation and mate choice.
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The Role of Morphometrics and Cladistics in the Taxonomy of Fossils: A Paleornithological Example
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Ramphastosula (Aves, Sulidae): A new genus from the Early Pliocene of the Pisco Formation, Peru
Article
  • Dec 2004
Cranial material from a new genus (Ramphastosula) of Sulidae is described. The material comes from the Early–Lower Pliocene of the Pisco Formation of the central-southern coast of Peru. The skulls are characterized by (1) remarkable convex curvature of the dorsal surface and straight ventral surface of the rostrum, only with a curvature on the third anterior part and the tip of the bill; (2) well developed occipital and temporal regions; (3) broad opisthotic process projecting to the level of postorbital processes; (4) broad temporal fossa, and (5) flat braincase and robust frontal region.
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