findarticles.com
Auk, The, Jan 2002 by Barbosa, A, Merino, S, de Lope, F, Moller, A P
ABSTRACT.-Parasites may affect host behavior in a number of ways, including their locomotory performance. We investigated whether the number of holes produced by the feather louse (Myrsidea rustica) affected flight behavior in adult male Barn Swallows (Hirundo rustica) by video-taping flight performance of individuals during escape and level flight.
Percentage of time spent flapping during foraging flight was positively related to number of holes, but not to other flight parameters such as wingbeat frequency. These results suggest indirect effects of feather lice on host performance that must be considered together with effects of thermoregulation and feather breakage. This is the first report of an effect of parasite load on flight behavior.RESUMEN.-Los parasitos pueden afectar el comportamiento de sus hospederos de diferentes maneras entre las que se incluye la locomocion. Investigamos si el numero de agujeros en el plumaje producidos por el piojo de pluma Myrsidea rustica afecta el comportamiento de vuelo de machos adultos de Hirundo rustica durante el escape y la alimentation. El numero de agujeros producidos por los piojos estuvo relacionado positivamente con el porcentaje de tiempo empleado en vuelo batido, pero no se encontro ninguna relacion con otros parametros de vuelo tales como la frecuencia de batido de las alas. Estos resultados sugieren la existencia de efectos indirectos de los piojos de pluma sobre sus hospederos que deben considerarse junto con sus efectos sobre la termorregulacion y el plumaje. Esta es la primera vez que se encuentra un efecto de un parasito sobre el comportamiento de vuelo.
Parasites have numerous effects on behavior, life history, and ecology of their hosts (e.g. Price 1980, Clayton and Moore 1997). Many studies have shown that parasites can change host behavior and thereby influence host fitness (Price 1980, Dobson 1988, Poinar 1991). However, most studies of host-parasite interactions have focused on life-history components such as reproductive success, quality of offspring or survival (see review in Moller 1997), sexual selection (Hamilton and Zuk 1982, Read 1988, Clayton 1991), dispersal (Brown and Brown 1992), and habitat selection (Emlen 1986, Chapman and George 1991). All those effects of parasites on host fitness are mediated by behavioral mechanisms that cause differences in performance. However, only very few studies have investigated the direct effect of parasites on locomotor performance of hosts, and those studies have exclusively been done on reptiles (Daniels 1985, Oppliger et al. 1996). This lack of information is all the more surprising given the importance of locomotion in efficient foraging and successful escape from predators (Webb 1986, Barbosa and Moreno 1999). As far as we know, effects of parasites on flight performance in birds have never been studied, although flight performance is one of the main ecological factors affecting bird life (Norberg 1990).
The feather louse (Myrsidea rustica) is abundant on adult and nestling Barn Swallows (Hirundo rustica; Moller 1994). This feather louse produces small holes in feathers causing damage to the plumage (Clayton 1991, Kose and Moller 1999). Feather lice have no effect on reproductive success of their hosts due to their vertical transmission and hence low level of virulence (Clayton and Tompkins 1995, Tompkins et al. 1996). However, feather lice have been found to indirectly affect thermoregulation and feather quality of avian hosts (Booth et al. 1993, Kose and Moller 1999). Although it has been suggested that parasites potentially may affect flight performance of avian hosts (Moller 1994), that possibility has not yet been tested.
The aim of this paper is to investigate whether the number of holes produced by the Myrsidea rustica affected flight behavior in adult male Barn Swallows. The Barn Swallow is a good model to test those relationships because it spends a large amount of time in flight while foraging.
Methods.-The study was carried out during the breeding season in 1997 in a colony of Barn Swallows located in the surroundings of Badajoz (38 deg 50’N, 6 deg 59’W), Spain, where colonies are located in rural buildings. Barn Swallows were captured in mist nets and we measured a number of morphological characters including length of outermost tail feathers, wingspan, and body mass.
During spring 1997, we filmed 25 male Barn Swallows released by hand (see Jones 1986 for a similar approach). Birds were previously captured and color-marked with color rings to provide easy identification. Several aspects of flight behavior were measured: (a) time taken to reach level flight (escape flight); (b) wingbeat frequency during escape flight until level flight was reached; (c) wingbeat frequency during level flight (foraging flight); and (d) percentage of total time flapping during foraging flight.
Timing of different kinds of flight mode (flapping and gliding) and wingbeat frequency was carried out in a magnetoscope using the frame by frame utility. Wingbeat frequency was determined by counting number of wingbeat cycles and measuring time taken (see Pennycuick 1990, Warrick 1998). Flight parameters (see below) were similar to those published by other authors (20% gliding flight; Turner 1980; 8.18 Hz wingbeat frequency; Warrick 1998), indicating reliability of our measurements of flight behavior. Moreover, when birds reached level flight, they immediately began to forage indicating that measurements during level flight were a reliable measure of foraging flights.
Myridisea rustica were counted on the basis of the number of holes in tail feathers. Estimated number of holes produced by lice in the tail is strongly positively related to the total load of lice obtained from extraction with chloroform vapor, indicating that holes in feathers provide a reliable estimate of Mallophaga abundance (Moller 1991).
Results.-The raw data of flight of male Barn Swallows are as follows: time to take-off (x(overscore) = 5.39 s, SE = 0.27), wingbeat frequency during take-off (x(overscore) = 8.06 Hz, SE = 0.20), wingbeat frequency during level flight (x(overscore) = 6.51 Hz, SE = 0.16), percentage of time flapping (x(overscore) = 88.2, SE = 1.82), and percentage of time gliding (x(overscore) = 11.8, SE = 1.82). Feather lice were present on 13 (52%) of the birds sampled with a mean number of holes = 9.6, SE = 1.58.
No significant relationship was found between number of holes produced by lice and the morphological variables measured (wingspan, F = 0.17, df = 1 and 23, r^sup 2^ = 0.007, P = 0.68; tail length, F = 2.68, df =land 23, r^sup 2^ = 0.10, P = 0.11).Results showed a positive and significant relationship between percentage of time in flapping flight and number of holes produced by lice (F = 5.35, df = 1 and 23, r^sup 2^ = 0.17, P = 0.03,). Other flight variables did not show any significant relationship with number of holes (time to take-off, F = 0.01, df = 1 and 23, r^sup 2^ = 0.0004, P = 0.91; wingbeat frequency at take-off, F = 0.06, df = 1 and 23, r^sup 2^ = 0.0025, P = 0.79; wingbeat frequency at level flight, F = 0.003, df = 1 and 23, r^sup 2^ = 0.0001, P = 0.95). As flight behavior could also be affected by variation in morphology among individuals (A. Barbosa unpubl. data), we performed a stepwise multiple regression analysis between percentage of time flapping and morphological variables (tail, wingspan, and body mass) and number of holes produced by lice. We found that only body mass and number of holes showed significant positive relationships with percentage of time flapping flight (partial correlation, body mass, r = 0.67, P
Discussion.-As far as we know, this is the first study investigating the relationship between parasites and flight performance in birds. Our results showed that individuals with high number of holes produced by lice spent a higher proportion of time in flapping flight during level flight, but no significant relationship was found between number of holes and wingbeat frequency or with flight behavior during escape flight. These results suggest that holes produced by lice did not produce mechanical constraints to flight. Variation in flight behaviour could be due to indirect effects.
The main effect of feather lice on their bird hosts is feather damage (Clayton 1991). Feather damage caused by Mallophaga can cause feather breakage (Kose and Moller 1999), which also may affect flight. However, none of the birds in our sample suffered from feather breakage when filmed, and effects of Mallophaga on flight behavior through breakage can therefore be excluded as an explanation for our results.Another effect of feather damage is increase of thermoregulation costs (Clayton 1991, Booth et al. 1993). Booth et al. (1993) found that Rock Doves (Columba livia) with high parasite loads suffered a reduction in body mass, and they suggested that fat reserves were used to cope with elevated metabolic rates of individuals with high parasite loads. If that were also the case in Barn Swallows, individuals with a high parasite load would have to increase their foraging efficiency through an increase in flapping flight to balance the extra metabolic cost due to Mallophaga. Barn Swallows forage on the wing, selecting large actively flying Diptera, which constitute their optimal diet (Turner 1982). Barn Swallows use flapping flight to capture such optimal prey (Turner 1980), whereas gliding is used mainly to save energy during flight, as in other birds (Norberg 1990).
On the other hand, lice load could indicate a poor condition of birds due to other factors (Potti and Merino 1995). In such cases birds could also increase foraging efficiency by trying to increase their condition. Changes in foraging behavior to increase foraging efficiency have been reported in parasitized fishes, even to the point of increasing predation risk (Milinski 1993).
Our study recorded a novel indirect effect of feather lice on their hosts, because abundance of feather lice estimated by the number of holes produced was related to flight behavior. This does not preclude direct effects of Mallophaga on the flight behavior of hosts through feather breakage, although that possibility remains to be tested.Acknowledgments.-A.B. was supported by a Marie Curie grant from the European Union and by a grant from the Direccion General de Ensenanza, Universidades e Investigation from the Junta de Extremadura (TEM98212) during field work and by Direction General de Ensenanza Superior project PB 98-0506 during writing. S.M. was supported by a postdoctoral grant of the Spanish Ministry of Education. Ed.L. was supported by grants for the Spanish Ministry of Science and Technology BOS 2000-0293 and Junta de Extremadura IPR00A021, and A.PM. was supported by an ATIPE BLANCHE from Centre National de la Recherche Scientifique.
LITERATURE CITED
BARBOSA, A., AND E. MORENO. 1999. Hindlimb morphology and locomotor performance in waders. An evolutionary approach. Biological Journal of the Linnean Society 67:313-330.
BOOTH, D. T., D. H. CLAYTON, AND B. A. BLOCK. 1993. Experimental demonstration of the energetic cost of parasitism in free-ranging hosts. Proceedings of the Royal Society of London, Series B 253:125-129.
BROWN, C. R., AND M. B. BROWN. 1992. Ectoparasitism as a cause of natal dispersal in Cliff Swallows. Ecology 73:1718-1723.
CHAPMAN, B. R., AND J. E. GEORGE. 1991. The effects of ectoparasites on Cliff Swallow growth and survival. Pages 69-92 in Bird-Parasite Interac
tions: Ecology, Evolution, and Behaviour (J. E. Loye and M. Zuk, Eds.). Oxford University Press, Oxford.
CLAYTON, D. H. 1991. The influence of parasites on host sexual selection. Parasitology Today 7:329– 334.
CLAYTON, D. H., AND J. MOORE. 1997. Host-Parasite Evolution. General Principles and Avian Models. Oxford University Press, Oxford.
CLAYTON, D. H., AND D. M. TOMPKINS. 1995. Comparative effects of mites and lice on the reproductive success of Rock Doves (Columba livia). Parasitology 110:195-206.
DANIELS, C. B. 1985. The effect of infection by a parasitic worm on swimming and diving in the water skink. Journal of Herpetology 19:160-162.
DOBSON, A. P. 1988. The population biology of parasite-induced changes in host behavior. Quarterly Review of Biology 63:139-365.
EMLEN, J. T. 1986. Responses of breeding Cliff Swallows to nidicolous parasite infestations. Condor 88:110-111.
HAMILTON, W. D., AND M. ZUK. 1982. Heritable true fitness and bright birds: A role for parasites? Science 218:384-387.
JONES, G. 1986. Sexual chases in Sand Martins (Riparia riparia): Cues for males to increase their reproductive success. Behavioral Ecology and Sociobiology 19:179-185.
KOSE, M., AND A. P. MOLLER. 1999. Sexual selection, feather breakage and parasites: The importance of white spots in the tail of the Barn Swallow. Behavioral Ecology and Sociobiology 45:430436.
MILINSKI, M. 1993. Predation risk and feeding behavior. Pages 285-305 in Behavior of Teleost Fishes (T. J. Pitcher, Ed.). Chapman and Hall, London.
MOLLER, A. P. 1991. Parasites, sexual ornaments, and mate choice in the Barn Swallow. Pages 328-348 in Bird-Parasite Interactions: Ecology, Evolution, and Behaviour (J. E. Loye and M. Zuk, Eds.). Oxford University Press, Oxford.MOLLER, A. P. 1994. Sexual Selection and the Barn Swallow. Oxford University Press, Oxford.
MOLLER, A. P. 1997. Parasitism and the evolution of host life history. Pages 105-127 in Host-Parasite Evolution. General Principles and Avian Models (D. H. Clayton and J. Moore, Eds.). Oxford University Press, Oxford.
NORBERG, U. M. 1990. Vertebrate Flight. SpringerVerlag, Berlin.
OPPLIGER, A., M. L. CELERIER, AND J. CLOBERT. 1996.
Physiological and behavioral changes in common lizards parasitized by haemogregarines. Parasitology 113:433-438.
PENNYCUICK, C. J. 1990. Predicting wingbeat frequency and wavelength of birds. Journal of Experimental Biology 150:171-185.
PONAR, G.O., JR. 1991. Hairworm (Nematomorpha: Gordioidea) parasites of New Zealand wetas (Orthoptera: Stenopelmatidae). Canadian Journal of Zoology 69:1592-1599.
POTTI, J., AND S. MERINO.1995. Louse loads of Pied Flycatchers: Effects of host’s sex, age condition and relatedness. Journal of Avian Biology 26: 203-208.
POTTI, J., AND S. MERINO. 1995. Louse loads of Pied Flycatchers: Effects of host’s sex, age conditon and relatedness. Journal of Avain Biology 26: 203-208.
PRICE, P.W. 1980. Evolutionary Biology of Parasites. Princeton University Press, Princeton, New Jersey.
READ, A.F. 1988. Sexual selection and the role of parasites. Trends in Ecology and Evolution 3:97– 102.
TOMPKINS, D.M., T. JONES, AND D.H. CLAYTON. 1996. Effect of vertically transmitted ectoparasites on the reproductive success of Swifts (Apus apus). Functional Ecology 19:733-740.
TURNER, A.K. 1980. The use of time and energy by aerial feeding birds. Ph.D. dissertation, University of Stirling, Stirling, United Kingdom.TURNER, A.K. 1982. Optimal foraging by the swallow: Prey size selection. Animal Behaviour 30: 862-872.
WARRICK, D.R. 1998. The turning- and linear- maneuvering performance of birds: The cost of efficiency for coursing insectivores. Canadian Jouranl of Zoology 76:1063-1079.
WEBB, P. W. 1986. Locomotion and predator-prey relationships. Pages 24-41 in Adaptation (G.V. Lauder and M.E. Feder, Eds.) University of Chicago Press, Chicago.
Received 27 November 2000, accepted 17 July 2001.
Associate Editor: F. Moore
A. BARBOSA,1,5 S. MERINO,2 F. DE LOPE,3 AND A.P. MOLLER4
1Estacion Experimental de Zonas Aridar, CSIC, C/General Segura, 1, E-04001 Alemeria, Spain;
2Department de Ecologia Evolutia, Museo Nacional de Ciencias Naturales, CSIC, C/Jose Gutierrez AbasCal, 2, E-28006 Madrid, Spain;
3Departmento de Biologia Animal, Facultad de Biologia, Universidad de Extremadura, Avda de Elvas s/n, E-06071 Badajoz, Spain; and
4Laboratorie d’ Ecologie, CNRS-URA 258, Universite Pierre et Marie Curie, Bat A 7e etage, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 05, France
5E-mail: barbosa7eeza.csic.es
Copyright American Ornithologists’ Union Jan 2002
Provided by ProQuest Information and Learning Company. All rights Reserved
• Growth and development of prefledging Canada Geese and Lesser Snow Geese: Ecological adaptation of physiological constraint?
by Badzinski, Shannon S
• Energetic consequences of clutch temperature and clutch size for a uniparental intermittent incubator: The Starling
by Reid, J M
• Importance of seed ingestion to an avian frugivore: An experimental approach to fruit choice based on seed load
by Stanley, Margaret C
• Diagnosability versus mean differences of Sage Sparrow subspecies
by Patten, Michael A
• Orientation of nocturnally migrating Swainson’s Thrush at dawn and dusk: Importance of energetic condition and geomagnetic cues
by Sandberg, Roland
• Elliott Coues Award, 2001: Raymond A. Paynter, Jr., and Melvin A Traylor, Jr
• Raptor migration in Israel and the Middle East: A summary of 30 years of field research
by Lott, Casey A
• Manakins (Pipridae) in second-growth and old-growth forests: Patterns of habitat use, movement, and survival
by Blake, John G
• Landbird counting techniques current practices and an alternative
by Rosenstock, Steven S
• Seabird supertrees: Combining partial estimates of procellariiform phylogeny
by Kennedy, Martyn
• Marion Jenkinson AOU Service Award, 2001: Ned K. Johnson
• Effects of hardwood reduction on winter birds in northwest Florida longleaf pine sandhill forests
by Provencher, Louis
• Towards reliable bird surveys: Accounting for individuals present but not detected
by Thompson, William L
• Bird Station Manual
by Pyle, Peter
• Double sampling to estimate density and population trends in birds
by Bart, Jonathan
• Maternal condition and nestling sex ratio in House Wrens
by Whittingham, Linda A
• Habitat use and breeding distribution of Magellanic Penguins in Northen San Jorge Gulf, Patagonia, Argentina
by Borboroglu, Pablo Garcia
• Brown-headed Cowbird parasitism of Ovenbirds in suburban forest fragments
by Hersek, Marta J
• Plasma amino acid concentrations as an indicator of protein availability to breeding Herring Gulls (Larus argentatus)
by Hebert, Craig E
• Composition and growth of King Eider ducklings in relation to egg size
by Anderson, Vanessa R
• Birds of British Columbia, Volume 4–Wood-Warblers through Old World Sparrows
by Walters, Eric L
• On grassland bird conservation in the northeast
by Norment, Christopher
• Continuous laying and clutch-size limitation in Mallards
by Arnold, Todd W
• Scales of food availability for an endangered insectivore, the Hawaii Akepa
by Fretz, J Scott
• Takahe: Fifty Years of Conservation Management and Research, The
by Wallace, George E
• Birds of New Guinea and the Bismarck Archipelago. A Photographic Guide
by LeCroy, Mary
• Density-dependent mass gain by Wilson’s Warblers during Stopover
by Kelly, Jeffrey F
• Trogons and Quetzals of the World
by Wenny, Dan
• William Brewster Memorial Award, 2001: Stephen I Rothstein
• Nocturnal heterothermy and torpor in the Malachite Sunbird (Nectarinia famosa)
by Downs, Colleen T
• Patterns of consumption and diet differentiation for three breeding warbler species during a spruce budworm outbreak
by McMartin, B
• Wood thrush movements and habitat use: Effects of forest management for Red-cockaded Woodpeckers
by Lang, Jason D
• Annual survival rates of wintering sparrows: Assessing demographic consequences of migration
by Sandercock, Brett K
• Bird Conservation on Golf Courses: A Design and Management Manual / Managing Wildlife Habitat on Golf Courses
by Main, Martin B
• Patterns of egg laying and breeding success in Humboldt Penguins (Spheniscus humboldti) at Punta San Juan, Peru
by Paredes, Rosana
• Effects of feather lice on flight behavior of male Barn Swallows (Hirundo rustica)
by Barbosa, A
• Why ornithologists should care about the theropod origin of birds
by Prum, Richard O
• Genetic parentage and mate guarding in the arctic-breeding Western Sandpiper
by Blomqvist, Donald
• Body condition and parental decisions in the Snow Petrel (Pagodroma nivea)
by Tveraa, Torkild
• 100 years ago in The American Ornithologists’ Union
