Tella et al 2015 Frontiers Ecol Environ

Parrots as overlooked seed dispersers S hortly after our friend and colleague Gary R Bortolotti passed away in 2011, his widow Heather Trueman sent JLT ten photographs of parrots that Gary had taken in Brazil. In one of these images, we saw a flying
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  338 ©The Ecological Society of America Parrots as overlooked seed dispersers S hortly after our friend and colleague Gary R Bortolottipassed away in 2011, his widow Heather Truemansent JLT ten photographs of parrots that Gary had takenin Brazil. In one of these images, we saw a flying chestnut-fronted macaw (  Ara severus ) carrying in its beak adefleshed fruit of the motacú palm (  Attalea phalerata ;upper-right arrow in Figure 1); upon enlarging this pic-ture for publication in Frontiers , we noticed anothermacaw transporting a smaller-sized seed (lower-left arrowin Figure 1). Gary’s photograph had captured what hasbeen described as an unusual behavior: active seed disper-sal by parrots. The unexpected nature of this observationwas reinforced during discussions with colleagues whospecialize in avian frugivory and seed dispersal. As theyargued – and contrary to well-recognized avian seed dis-persers such as frugivorous passerines, trogons, and tou-cans, which typically swallow whole fruits and disperseseeds after gut passage – parrots handle and destroy fruitsin situ to eat the pulp or to gain access to the seeds.Although more than 400 known species of parrot inhabitthe world’s tropical ecosystems, only lesser vasa parrots( Coracopsis nigra ; Böhning-Gaese et al . 1999) and plainparakeets ( Brotogeris tirica ; Sazima 2008) have previouslybeen reported to regularly disperse seeds transported intheir bills. This has led to the general assumption thatparrots are seed predators and thus do not participate inseed-dispersal mutualisms (Fleming and Kress 2013). Because only two parrot species were known to routinelycarry seeds in flight, this behavior is considered to beunusual. However, these two species are among the moreancestral ( Coracopsis ) and more modern ( Brotogeris )species within the phylogenetic tree of the Psittacidae fam-ily of parrots (Wright et al . 2008), suggesting that thisbehavior could be well-conserved through the evolutionand diversification of this large lineage of birds, butnonetheless overlooked. Parrots often forage in the canopyof tropical forests, and their foraging behaviors are difficultto study due to remote locations and logistical constraints.Thus, the likelihood of observing a parrot in flight carryinga fruit or seed in its bill may be low, and such behaviorsmay go largely unreported. A new photograph (Figure 2)taken by JLT, this time of a large flock of red-frontedmacaws (  Ara rubrogenys ) in Bolivia, led us to reconsiderthis second hypothesis. In this case, the transport of an earof corn ( Zea mays ) by a macaw went unseen until the pho-tograph was examined more closely. We then decided toreassess the foraging behavior of parrots, searching for indi-cations of other dispersal events.To that end, we joined a group of parrot biologists andecologists studying foraging behavior who, since 2012,have recorded hundreds of observations of parrots dis-persing fruits or seeds using their bills or, less often, theirfeet (WebFigure 1). Although preliminary, our data sug-gest that seed dispersal by parrots is not unusual.Observations came from 28 parrot species belonging to 16genera, ranging in body size from the smallest parakeetsto the largest macaws, and involved the dispersal of fruitsand seeds from 94 species of trees (including palms) andshrubs. Instances were recorded in seven countries(Argentina, Bolivia, Brazil, Chile, Ecuador, Peru, andSpain), comprising mostly neotropical parrots but also anAfrican and an Asian species from introduced popula-tions of parrots in Spain. They covered a wide variety of ecosystems – from the sea-level Argentinean Pampas tohigh-altitude Andean forests, fromcontinents to islands, from thewettest Amazonian savannas to thedriest Caatinga forests, and from pris-tine to urban habitats. Regardingfunctional interactions, parrots –regardless of their srcin – dispersedboth native and non-native (includ-ing cultivated) plants. We measured the distances thatfruits or seeds were carried by par-rots, with the aid of laser rangefind-ers, in 686 dispersal events. Giventhe long-distance flying abilities of most parrot species, the distancesspanned a wide range (maximum =1200 m, median = 27 m, mean = 44m; WebFigure 2). This indicates thatparrots may serve as efficient long-distance seed dispersers. Moreover,we observed several incidents wheretransported fruits or seeds were acci- NATURAL HISTORY NOTES NATURAL HISTORYNOTES  Figure 1. Chestnut-fronted macaws ( Ara severus ) transportin g a defleshed motacú palm fruit ( Attalea phalerata ; upper-right arrow) and an unidentified seed (lower-left arrow).Photo taken on 17 Oct 2009 (Rio Cristalino, Brazil).    G  a  r  y   R    B  o  r   t  o   l  o   t   t   i   JL Tella et al . Natural History Notes 339 © The Ecological Society of America  José L Tella 1* , Adrián Baños-Villalba 2 ,Dailos Hernández-Brito 1,2 , Abraham Rojas 3 ,Erica Pacífico 1,4 , José A Díaz-Luque 5 ,Martina Carrete 2 , Guillermo Blanco 6 ,and Fernando Hiraldo 1 1 Estación Biológica de Doñana (CSIC), Sevilla, Spain * (; 2 University Pablo de Olavide, Sevilla,Spain; 3 Museo de Historia Natural Noel Kempf Mercadoand Zoológico Municipal, Santa Cruz de la Sierra, Bolivia; 4 Museu de Zoologia, Universidade de São Paulo, São Paulo,Brazil; 5 Proyecto de Conservación Paraba Barba Azul, World Parrot Trust, Beni, Bolivia; 6 Museo Nacional de Ciencias Naturales (CSIC),Madrid, Spain    J  o  s   é   L   T  e   l   l  a dentally dropped in flight or whenthe parrot perched during eating.Importantly, we often found uneaten,ripened seeds and seedlings growingunder tree perches used by parrots, farfrom the nearest plant that couldhave provided those seeds. All of these observations point to parrots asgenuine, but thus far overlooked,seed dispersers.This short story illustrates howserendipitous photographic evidencecan lead scientists to question whathas been considered unusual or diffi-cult-to-observe behaviors, and high-lights how much we have yet to learnabout the natural history of mostorganisms. Given that parrots arelarge, colorful, and loud birds thathave attracted the attention andcompany of humans for centuries(Tella and Hiraldo 2014), how manysmall yet important life-history detailsare we missing about numerous other, perhaps less charis-matic, species? The net effect of parrots on the popula-tion dynamics of their food plants relies on the negativeimpact of seed predation versus the benefits for thegenetic structure of tropical forests derived from long-dis-tance seed dispersal. This contribution of parrots asantagonists and mutualists with respect to their diversefood plants warrants further research. The fact that one-third of parrot species in the world are threatened withextinction should urge the assessment of their ecologicalroles and the ecosystem-wide consequences of parrotpopulation declines. Parrots may play a key role in thefunctioning and maintenance of biodiversity not only intropical ecosystems but also in regions where parrots havebeen introduced.Gary’s photograph presented us with an enlighteningmoment in our own research, and we hope that the pre-liminary data discussed here will encourage otherresearchers to more thoroughly explore the role of parrotsin providing a key ecosystem service as seed dispersers.   Acknowledgements Gary R Bortolotti inspired us to explore this parrotbehavior as well as many other aspects of avian behaviorand ecology. Preliminary results on parrot seed dispersalwere obtained through projects funded by FundaciónBiodiversidad, Fundación Repsol, World Parrot Trust,and a Severo Ochoa award (to FH), and discussed withinthe ParrotNet COST Action group.  References Böhning-Gaese K, Gaese BH, and Rabemanantsoa SB. 1999.Importance of primary and secondary seed dispersal in theMalagasy tree Commiphora guillaumini. Ecology 80 : 821–32.Fleming TH and Kress WJ. 2013. The ornaments of life. Chicago,IL: University of Chicago Press.Sazima I. 2008. The parakeet Brotogeris tirica feeds on and dispersesthe fruits of the palm Syagrus romanzoffiana in southeasternBrazil. Biota Neotropica 8 : 231–34.Tella JL and Hiraldo F. 2014. Illegal and legal parrot trade shows along-term, cross-cultural preference for the most attractivespecies increasing their risk of extinction. PLoS ONE 9 :e107546.Wright TF, Schirtzinger EE, Matsumoto T, et al . 2008. A multilocusmolecular phylogeny of the parrots (Psittaciformes): supportfor a Gondwanan srcin during the Cretaceous. Mol Biol Evol 25 : 2141–56.  Figure 2. Red-fronted macaw ( Ara rubrogenys ) transporting an ear of corn ( Zeamays ). Photo taken on 27 Aug 2011 (Los Negros, Bolivia).  © The Ecological Society of America  JL Tella et al . – Supplemental information  WebFigure 1. Lear’s macaw ( Anodorhynchus leari ) transporting several licuri palm ( Syagrus coronata ) fruits with its feet. Photo taken on 25 Feb 2013(Canudos, Brazil).    J  o   ã  o   M    R  o  s  a  WebFigure 2. Distribution of distances ( n = 686) at which 28 species of parrotsmoved whole fruits or seeds from the mother plant to perching trees. Several data points correspond to minimum dispersal distances, when flying parrots were out of sight in the forests.
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