Skip to main content
SpringerLink
Log in

Cognitive skills and bacterial load: comparative evidence of costs of cognitive proficiency in birds

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

Parasite-mediated selection may affect the evolution of cognitive abilities because parasites may influence development of the brain, but also learning capacity. Here, we tested some predictions of this hypothesis by analyzing the relationship between complex behaviours (feeding innovations (as a measure of behavioural flexibility) and ability to detect foreign eggs in their nests (i.e. a measure of discriminatory ability)) and abundance of microorganisms in different species of birds. A positive relationship would be predicted if these cognitive abilities implied a larger number of visited environments, while if these skills favoured detection and avoidance of risky environments, a negative relationship would be the prediction. Bacterial loads of eggshells, estimated for mesophilic and potentially pathogenic bacteria (i.e. Enterococcus, Staphylococcus and Enterobacteriaceae), were used as a surrogate of probability of contact with pathogenic bacteria. We found that bird species with higher feeding innovation rates and rejection rates of experimental brood parasitic eggs had higher density of bacteria on their eggshells than the average species. Since the analysed groups of microorganisms include pathogenic bacteria, these results suggest that both feeding innovation and ability to recognize foreign eggs are costly and highlight the importance of parasite-mediated selection in explaining the evolution of cognitive abilities in animals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aiello LC, Wheeler P (1995) The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr Anthropol 36:199–221

    Google Scholar 

  • Alghamdi A, Raine NE, Rosato E, Mallon EB (2009) No evidence for an evolutionary trade-off between learning and immunity in a social insect. Biol Lett 5:55–57

    PubMed  CAS  Google Scholar 

  • Alvarez F (1999) Attractive non-mimetic stimuli in cuckoo Cuculus canorus eggs. Ibis 141:142–144

    Google Scholar 

  • Amundsen T, Brobakken PT, Moksnes A, Røskaft E (2002) Rejection of common cuckoo Cuculus canorus eggs in relation to female age in the bluethroat Luscinia svecica. J Avian Biol 33:366–370

    Google Scholar 

  • Antonov A, Stokke BG, Moksnes A, Røskaft E (2006a) Coevolutionary interactions between common cuckoos and corn buntings. Condor 108:414–422

    Google Scholar 

  • Antonov A, Stokke BG, Moksnes A, Røskaft E (2006b) Egg rejection in marsh warblers (Acrocephalus palustris) heavily parasitized by common cuckoos (Cuculus canorus). Auk 123:419–430

    Google Scholar 

  • Antonov A, Stokke BG, Moksnes A, Kleven O, Honza M, Røskaft E (2006c) Eggshell strength of an obligate brood parasite: a test of the puncture resistance hypothesis. Behav Ecol Sociobiol 60:11–18

    Google Scholar 

  • Antonov A, Stokke BG, Moksnes A, Røskaft E (2009) Evidence for egg discrimination preceding failed rejection attempts in a small cuckoo host. Biol Lett 5:169–171

    PubMed  Google Scholar 

  • Antonov A, Stokke BG, Ranke PS, Fossøy F, Moksnes A, Røskaft E (2010) Absence of egg discrimination in a suitable cuckoo Cuculus canorus host breeding away from trees. J Avian Biol 41:501–504

    Google Scholar 

  • Atlas RM, Bartha R (2001) Ecología microbiana y microbiología ambiental. Addison Wesley Longman, Inc., Madrid

    Google Scholar 

  • Avilés JM, Garamszegi LZ (2007) Egg rejection and brain size among potential hosts of the common cuckoo. Ethology 113:562–572

    Google Scholar 

  • Bartol I, Moskat C, Karcza Z, Kisbenedek T (2003) Great reed warblers bury artificial objects, not only cuckoo eggs. Acta Zool Acad Sci Hung 49:111–114

    Google Scholar 

  • Board RG, Clay C, Lock J, Dolman J (1994) The egg: a compartmentalized, aseptically packaged food. In: Board RG, Fuller R (eds) Microbiology of the avian egg. Chapman & Hall, London, pp 43–62

    Google Scholar 

  • Brooke MdL, Davies NB, Noble DG (1998) Rapid decline of host defenses in response to reduced cuckoo parasitism: behavioral flexibility of reed warblers in a changing world. Proc R Soc Lond B 265:1277–1282

    Google Scholar 

  • Bruce J, Drysdale EM (1994) Trans-shell transmission. In: Board RG, Fuller R (eds) Microbiology of avian eggs. Chapman & Hall, London, pp 63–91

    Google Scholar 

  • Burns JG, Foucaud J, Mery F (2011) Costs of memory: lessons from ‘'mini’ brains. Proc R Soc B. doi:10.1098/rspb.2010.2488:

  • Clark L, Mason JR (1985) Use of nest material as insecticidal and anti-pathogenic agents by the European starling. Oecologia 67:169–176

    Google Scholar 

  • Clark L, Mason JR (1988) Effect of biologically active plants used as nest material and the derived benefit to starling nestlings. Oecologia 77:174–180

    Google Scholar 

  • Cook MI, Beissinger SR, Toranzos GA, Rodriguez RA, Arendt WJ (2003) Trans-shell infection by pathogenic micro-organisms reduces the shelf life of non-incubated bird's eggs: a constraint on the onset of incubation? Proc R Soc Lond B 270:2233–2240

    Google Scholar 

  • Cook MI, Beissinger SR, Toranzos GA, Arendt WJ (2005a) Incubation reduces microbial growth on eggshells and the opportunity for trans-shell infection. Ecol Lett 8:532–537

    PubMed  Google Scholar 

  • Cook MI, Beissinger SR, Toranzos GA, Rodriguez RA, Arendt WJ (2005b) Microbial infection affects egg viability and incubation behavior in a tropical passerine. Behav Ecol 16:30–36

    Google Scholar 

  • Davies NB, Brooke MdL (1989) An experimental study of coevolution between the cuckoo, Cuculus canorus, and its host. I. Host egg discrimination. J Anim Ecol 58:207–224

    Google Scholar 

  • Davies NB, MdL B, Kacelnik A (1996) Recognition errors and probability of parasitism determine whether reed warblers should accept or reject mimetic cuckoo eggs. Proc R Soc Lond B 263:925–931

    Google Scholar 

  • Franz CMAP, Holzapfel WH, Stiles ME (1999) Enterococci at the crossroads of food safety? Int J Food Microbiol 47:1–24

    PubMed  CAS  Google Scholar 

  • Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726

    PubMed  CAS  Google Scholar 

  • Garamszegi LZ, Møller AP (2010) Effects of sample size and intraspecific variation in phylogenetic comparative studies: a meta-analytic review. Biol Rev 4:797–805

    Google Scholar 

  • Garamszegi LZ, Erritzøe J, Møller AP (2007) Feeding innovations and parasitism in birds. Biol J Linn Soc 90:441–455

    Google Scholar 

  • Garamszegi LZ, Eens M, Erritzoe J, Møller AP (2005) Sexually size dimorphic brains and song complexity in passerine birds. Behav Ecol 16:335–345

    Google Scholar 

  • Grim T, Honza M (2001) Differences in behaviour of closely related thrushes (Turdus philomelos and T merula) to experimental parasitism by the common cuckoo Cuculus canorus. Biologia 56:549–556

    Google Scholar 

  • Guigueno MF, Sealy SG (2009) Nest sanitation plays a role in egg burial by yellow warblers. Ethology 115:247–256

    Google Scholar 

  • Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han KL, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768

    PubMed  CAS  Google Scholar 

  • Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

    Google Scholar 

  • Honza M, Prochazka P, Stokke BG, Moksnes A, Røskaft E, Capek M, Mrlik V (2004) Are blackcaps current winners in the evolutionary struggle against the common cuckoo? J Ethol 22:175–180

    Google Scholar 

  • Houston CS, Saunders JR, Crawford RD (1997) Aerobic bacterial flora of addled raptor eggs in Saskatchewan. J Wildl Dis 33:328–331

    PubMed  CAS  Google Scholar 

  • Iwaniuk AN, Nelson JE (2003) Developmental differences are correlated with relative brain size in birds: a comparative analysis. Can J Zool 81:1913–1928

    Google Scholar 

  • Järvinen A (1984) Relationship between the common cuckoo Cuculus canorus an its host, the redstart Phoenicurus phoenicurus. Ornis Fenn 61:84–88

    Google Scholar 

  • Jønsson KA, Fjeldså J (2006) A phylogenetic supertree of oscine passerine birds (Aves: Passeri). Zool Scripta 35:149–186

    Google Scholar 

  • Krieg NR, Holt JG (1984) Bergey's manual of systematic bacteriology. Williams & Wilkins, Baltimore, Maryland

    Google Scholar 

  • Lefebvre L, Bolhuis JJ (2003) Positive and negative correlates of feeding innovation in birds: evidence for limited modularity. In: Reader SM, Laland KN (eds) Animal innovation. Oxford University Press, Oxford, pp 39–61

    Google Scholar 

  • Lefebvre L, Whittle P, Lascaris E, Finkelstein A (1997) Feeding innovations and forebrain size in birds. Anim Behav 53:549–560

    Google Scholar 

  • Lefebvre L, Juretic N, Nicolakakis N, Timmermans S (2001) Is the link between forebrain size and feeding innovations caused by confounding variables? A study of Australian and North American birds. Anim Cogn 4:91–97

    Google Scholar 

  • Lefebvre L, Nicolakakis N, Boire D (2002) Tools and brains in birds. Behaviour 139:939–973

    Google Scholar 

  • Lefebvre L, Reader SM, Sol D (2004) Brains, innovations and evolution in birds and primates. Brain Behav Evol 63:233–246

    PubMed  Google Scholar 

  • Lindholm AK, Thomas RJ (2000) Differences between populations of reed warblers in defences against brood parasitism. Behaviour 137:25–42

    Google Scholar 

  • Lotem A (1993) Learning to recognize nestling is maladaptive for cuckoo Cuculus canorus host. Nature 362:743–745

    Google Scholar 

  • Lotem A, Nakamura H, Zahavi A (1995) Constraints on egg discrimination and cuckoo host coevolution. Anim Behav 49:1185–1209

    Google Scholar 

  • Lovaszi P, Moskat C (2004) Break-down of arms race between the red-backed shrike (Lanius collurio) and common cuckoo (Cuculus canorus). Behaviour 141:245–262

    Google Scholar 

  • Lozano GA (1998) Parasitic stress and self-medication in wild animals. Adv Stud Behav 27:291–317

    Google Scholar 

  • Lyon BE (2003) Egg regognition and counting reduce costs of avian conspecific brood parasitism. Nature 422:495–499

    PubMed  CAS  Google Scholar 

  • Mallon EB, Brockmann A, Schmid-Hempel P (2003) Immune response inhibits associative learning in insects. Proc R Soc Lond B 270:2471–2473

    Google Scholar 

  • Martin TE, Møller AP, Merino S, Clobert J (2001) Does clutch size evolve in response to parasites and immunocompetence? Proc Natl Acad Sci USA 98:2071–2076

    PubMed  CAS  Google Scholar 

  • Martín-Vivaldi M, Soler M, Møller AP (2002) Unrealistically high costs of rejecting artificial model eggs in cuckoo Cuculus canorus hosts. J Avian Biol 33:295–301

    Google Scholar 

  • Martín-Vivaldi M, Ruiz-Rodríguez M, Mendez M, Soler JJ (2006) Relative importance of factors affecting nestling immune response differs between junior and senior nestlings within broods of hoopoes Upupa epops. J Avian Biol 37:467–476

    Google Scholar 

  • Martín-Vivaldi M, Peña A, Peralta-Sánchez JM, Sánchez L, Ananou S, Ruiz-Rodríguez M, Soler JJ (2010) Antimicrobial chemicals in hoopoe preen secretions are produced by symbiotic bacteria. Proc R Soc B 277:123–130

    PubMed  Google Scholar 

  • Martín-Vivaldi M, Soler JJ, Møller AP, Pérez-Contreras T, Soler M (2012) Importance of nest site and habitat in egg recognition ability of potential hosts of the European cuckoo Cuculus canorus. Ibis In press:

  • Matson KD, Ricklefs RE, Klasing KC (2005) A hemolysis–hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev Comp Imm 29:275–286

    CAS  Google Scholar 

  • McArthur JV (2006) Microbial ecology: an evolutionary approach. Elsevier Academic Press, Amsterdam

    Google Scholar 

  • Mennerat A, Mirleau P, Blondel J, Perret P, Lambrechts M, Heeb P (2009) Aromatic plants in nests of the blue tit Cyanistes caeruleus protect chicks from bacteria. Oecologia 161:849–855

    PubMed  Google Scholar 

  • Merino S, Potti J (1996) Weather dependent effects of nest ectoparasites on their bird hosts. Ecography 19:107–113

    Google Scholar 

  • Mlikovsky J (1989) Brain size in birds: 2. Falconiformes through Gaviiformes. Vest cs Spolec Zool 53:200–213

  • Moksnes A, Røskaft E, Braa AT, Korsnes L, Lampe HM, Pedersen HC (1991) Behavioural responses of potential hosts towards artificial cuckoo eggs and dummies. Behaviour 116:64–89

    Google Scholar 

  • Moksnes A, Røskaft E, Solli MM (1994) Documenting puncture ejection of parasitic eggs by chaffinches Fringilla coelebs and blackaps Sylvia atricapilla. Fauna Norvergica, Ser C, Cinclus 17:115–118

    Google Scholar 

  • Møller AP (1987) Egg predation as a selective factor for nest design: an experiment. Oikos 50:91–94

    Google Scholar 

  • Møller AP (1997) Parasitism and the evolution of host life history. In: Clayton DH, Moore J (eds) Host-parasite evolution: general principles and avian models. Oxford Univesity Press, Oxford, pp 105–127

    Google Scholar 

  • Møller AP, Erritzøe J (1998) Host immune defence and migration in birds. Evol Ecol 12:945–953

    Google Scholar 

  • Møller AP, Erritzøe J (2002) Coevolution of host immune defence and parasite-induced mortality: relative spleen size and mortality in altricial birds. Oikos 99:95–100

    Google Scholar 

  • Møller AP, Martín-Vivaldi M, Merino S, Soler JJ (2006) Density-dependent and geographical variation in bird immune response. Oikos 115:463–474

    Google Scholar 

  • Moreno J, Briones V, Merino S, Ballesteros C, Sanz JJ, Tomás G (2003) Beneficial effects of cloacal bacteria on growth and fledging size in nestling pied flycatchers (Ficedula hypoleuca) in Spain. Auk 120:784–790

    Google Scholar 

  • Moskat C, Fuisz TI (1999) Reactions of red-backed shrikes Lanius collurio to artificial cuckoo Cuculus canorus eggs. J Avian Biol 30:175–181

    Google Scholar 

  • Moskat C, Karcza Z, Csörgö T (2003a) Egg rejection in European blackbirds (Turdus merula): the effect of mimicry. Ornis Fenn 80:86–91

    Google Scholar 

  • Moskat C, Szekely T, Kisbenedek T, Karcza Z, Bartol I (2003b) The importance of nest cleaning in egg rejection behaviour of great reed warblers Acrocephalus arundinaceus. J Avian Biol 34:16–19

    Google Scholar 

  • Narushin VG (2005) Production, modeling, and education: egg geometry calculation using the measurements of length and breadth. Poultry Sci 84:482–484

    CAS  Google Scholar 

  • Nicolakakis N, Lefebvre L (2000) Forebrain size and innovation rate in European birds: feeding, nesting and confounding variables. Behaviour 137:1415–1429

    Google Scholar 

  • Nicolakakis N, Sol D, Lefebvre L (2003) Behavioural flexibility predicts species richness in birds, but not extinction risk. Anim Behav 65:445–452

    Google Scholar 

  • Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211:1792–1804

    PubMed  CAS  Google Scholar 

  • Overington SE, Morand-Ferron J, Boogert NJ, Lefebvre L (2009) Technical innovations drive the relationship between innovativeness and residual brain size in birds. Anim Behav 78:1001–1010

    Google Scholar 

  • Pagel M (1997) Inferring evolutionary processes from phylogenies. Zool Scripta 26:331–348

    Google Scholar 

  • Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    PubMed  CAS  Google Scholar 

  • Palomino JJ (1997) Reproductive ecology and parental care in the rufous-tailed scrub-robin: responses to parasitism by cuckoo. PhD thesis University of Granada, Granada.

  • Payne RB (1977) The ecology of brood parasitism in birds. Ann Rev Ecol Syst 8:1–28

    Google Scholar 

  • Peralta-Sánchez JM (2011) Las bacterias como agentes modeladores de las estrategias vitales en aves. PhD thesis University of Granada, Granada.

  • Peralta-Sánchez JM, Møller AP, Martín-Platero AM, Soler JJ (2010) Number and colour composition of nest lining feathers predict eggshell bacterial community in barn swallow nests: an experimental study. Funct Ecol 24:426–433

    Google Scholar 

  • Playfair J, Bancroft G (2004) Infection and immunity. Oxford University Press, Oxford

    Google Scholar 

  • Pons JM, Hassanin A, Crochet PA (2005) Phylogenetic relationships within the Laridae (Charadriiformes: Aves) inferred from mitochondrial markers. Mol Phylogenet Evol 37:686–699

    PubMed  CAS  Google Scholar 

  • Prochazka P, Honza M (2003) Do common whitethroats (Sylvia communis) discriminate against alien eggs? J Ornithol 144:354–363

    Google Scholar 

  • Prochazka P, Honza M (2004) Egg discrimination in the yellowhammer. Condor 106:405–410

    Google Scholar 

  • Riddell CE, Mallon EB (2006) Insect psychoneuroimmunology: immune response reduces learning in protein starved bumblebees (Bombus terrestris). Brain Behav Immun 20:135–138

    PubMed  CAS  Google Scholar 

  • Rohwer S, Spaw CD, Røskaft E (1989) Cost to northern orioles of puncture-ejecting parasitic cowbird eggs from their nest. Auk 106:734–738

    Google Scholar 

  • Rothstein SI (1975a) An experimental and teleonomic investigation of avian brood parasitism. Condor 77:250–271

    Google Scholar 

  • Rothstein SI (1975b) Mechanisms of avian egg-recognition: do birds know their own eggs? Anim Behav 23:268–278

    Google Scholar 

  • Rothstein SI (1990) A model system for coevolution: avian brood parasitism. Ann Rev Ecol Syst 21:481–508

    Google Scholar 

  • Ruiz-Gonzalez MX, Brown MJF (2006) Honey bee and bumblebee trypanosomatids: specificity and potential for transmission. Ecol Entomol 31:616–622

    Google Scholar 

  • Ruiz-Rodriguez M, Lucas FS, Heeb P, Soler JJ (2009) Differences in intestinal microbiota between avian brood parasites and their hosts. Biol J Linn Soc 96:406–414

    Google Scholar 

  • Rutila J, Latja R, Koskela K (2002) The common cuckoo Cuculus canorus and its cavity nesting host, the redstart Phoenicurus phoenicurus: a peculiar cuckoo–host system? J Avian Biol 33:414–419

    Google Scholar 

  • Rutila J, Jokimäki J, Aviles JM, Kaisanlahti-Jokimaki ML (2006) Responses of parasitized and unparasitized common redstart (Phoenicurus phoenicurus) populations against artificial cuckoo parasitism. Auk 123:259–265

    Google Scholar 

  • Sæther SA, Grøtan V, Engen S, Noble DG, Freckleton RP (2011) Rarity, life history and scaling of the dynamics in time and space of British birds. J Anim Ecol 80:215–224

    PubMed  Google Scholar 

  • Sengupta B, Stemmler M, Laughlin SB, Niven JE (2010) Action potential energy efficiency varies among neuron types in vertebrates and invertebrates. PLoS Computational Biology 6:e1000840

    PubMed  Google Scholar 

  • Shizuka D, Lyon BE (2010) Coots use hatch order to learn to recognize and reject conspecific brood parasitic chicks. Nature 463:223–U108

    PubMed  CAS  Google Scholar 

  • Singleton DR, Harper RG (1998) Bacteria in old house wren nests. J Field Ornithol 69:71–74

    Google Scholar 

  • Sol D, Lefebvre L (2000) Behavioural flexibility predicts invasion success in birds introduced to New Zealand. Oikos 90:599–605

    Google Scholar 

  • Sol D, Timmermans S, Lefebvre L (2002) Behavioural flexibility and invasion success in birds. Anim Behav 63:495–502

    Google Scholar 

  • Sol D, Duncan RP, Blackburn TM, Cassey P, Lefebvre L (2005) Big brains, enhanced cognition, and response of birds to novel environments. Proc Natl Acad Sci USA 102:5460–5465

    PubMed  CAS  Google Scholar 

  • Soler JJ (1999) Do life-history variables of European cuckoo hosts explain their egg-rejection behavior? Behav Ecol 10:1–6

    Google Scholar 

  • Soler JJ, Avilés JM (2010) Sibling competition and conspicuousness of nestling gapes in altricial birds: a comparative study. PLoS One 5:e10509

    PubMed  Google Scholar 

  • Soler M, Møller AP (1990) Duration of sympatry and coevolution between the great spotted cuckoo and its magpie host. Nature 343:748–750

    Google Scholar 

  • Soler JJ, Møller AP (1996) A comparative analysis of the evolution of variation in appearance of eggs of European passerines in relation to brood parasitism. Behav Ecol 7:89–94

    Google Scholar 

  • Soler JJ, Martínez JG, Soler M, Møller AP (1999a) Genetic and geographic variation in rejection behavior of cuckoo eggs by European magpie populations: an experimental test of rejecter-gene flow. Evolution 53:947–956

    Google Scholar 

  • Soler JJ, Møller AP, Soler M (1999b) A comparative study of host selection in the European cuckoo Cuculus canorus. Oecologia 118:265–276

    Google Scholar 

  • Soler M, Martín-Vivaldi M, Pérez-Contreras T (2002) Identification of the sex responsible for recognition and the method of ejection of parasitic eggs in some potential common cuckoo hosts. Ethology 108:1093–1101

    Google Scholar 

  • Soler JJ, Martín-Vivaldi M, Ruiz-Rodríguez M, Valdivia E, Martín-Platero AM, Martínez-Bueno M, Peralta-Sánchez JM, Méndez M (2008) Symbiotic association between hoopoes and antibiotic-producing bacteria that live in their uropygial gland. Funct Ecol 22:864–871

    Google Scholar 

  • Soler JJ, Martín-Vivaldi M, Peralta-Sánchez JM, Ruiz-Rodríguez M (2010) Antibiotic-producing bacteria as a possible defence of birds against pathogenic microorganisms. Open Ornithol J 3:93–100

    Google Scholar 

  • Soler JJ, Peralta-Sánchez JM, Martínez Bueno M, Martín-Vivaldi M, Martín-Gálvez D, Vela AI, Briones V, Pérez-Contreras T (2011) Brood parasitism is associated with increased bacterial contamination of host eggs: bacterial loads of host and parasitic eggs. Biol J Linn Soc 103:836–848

    Google Scholar 

  • Stadelman WJ (1994) Contaminats of liquid eggs products. In: Board RG, Fuller R (eds) Microbiology of the avian egg. Chapman & Hall, London, pp 139–151

    Google Scholar 

  • Stokke BG, Moksnes A, Røskaft E, Rudolfsen G, Honza M (1999) Rejection of artificial cuckoo (Cuculus canorus) eggs in relation to variation in egg appearance among reed warblers (Acrocephalus scirpaceus). Proc R Soc Lond B 266:1483–1488

    Google Scholar 

  • Stokke BG, Hafstad I, Rudolfsen G, Moksnes A, Møller AP, Røskaft E, Soler M (2008) Predictors of resistance to brood parasitism within and among reed warbler populations. Behav Ecol 19:612–620

    Google Scholar 

  • Timmermans S, Lefebvre L, Boire D, Basu P (2000) Relative size of the hyperstriatum ventrale is the best predictor of feeding innovation rate in birds. Brain Behav Evol 56:196–203

    PubMed  CAS  Google Scholar 

  • Tucker GM, Heath MF (1994) Birds in Europe, their conservation status. BirdLife International, Cambridge

    Google Scholar 

  • Vas Z, Lefebvre L, Johnson KP, Reiczigel J, Rózsa L (2011) Clever birds are lousy: co-variation between avian innovation and the taxonomic richness of their amblyceran lice. Int J Parasitol 41:1295–1300

    PubMed  Google Scholar 

  • von Haartman L (1981) Co-evolution of the cuckoo Cuculus canorus and a regular cuckoo host. Ornis Fenn 58:1–10

    Google Scholar 

Download references

Acknowledgments

We would like to thank Rosario Millán for the technical assistance and Liesbeth de Neve, David Martín-Gálvez, María Roldán, Juan Rodríguez, Deseada Parejo, Magdalena Ruiz-Rodríguez, Carlos Navarro and Juan Diego Ibañez for sampling nests of some species. Funding was provided by Spanish Ministerio de Educación y Ciencia and European founds (FEDER) (CGL2007-61251 and CGL2010-19233-C03-01).

Author information

Authors and Affiliations

  1. Estación Experimental de Zonas Áridas (EEZA-CSIC), Almería, Spain

    Juan José Soler & Juan Manuel Peralta-Sánchez

  2. Grupo Coevolución, Unidad asociada al CSIC, Universidad de Granada, Granada, Spain

    Juan José Soler, Juan Manuel Peralta-Sánchez, Manuel Martín-Vivaldi & Antonio Manuel Martín-Platero

  3. Departamento de Biología Animal, Facultad de Ciencias, Universidad de Granada, Granada, Spain

    Manuel Martín-Vivaldi

  4. Departamento de Microbiología, Facultad de Ciencias, Universidad de Granada, Granada, Spain

    Antonio Manuel Martín-Platero

  5. Cypresvej 1, 9700, Brønderslev, Denmark

    Einar Flensted-Jensen

  6. Laboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud, Bâtiment 362, 91405, Orsay Cedex, France

    Anders Pape Møller

Authors
  1. Juan José Soler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan Manuel Peralta-Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Manuel Martín-Vivaldi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Antonio Manuel Martín-Platero
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Einar Flensted-Jensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anders Pape Møller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan José Soler.

Additional information

Communicated by: Alexandre Roulin

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 132 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Soler, J.J., Peralta-Sánchez, J.M., Martín-Vivaldi, M. et al. Cognitive skills and bacterial load: comparative evidence of costs of cognitive proficiency in birds. Naturwissenschaften 99, 111–122 (2012). https://doi.org/10.1007/s00114-011-0875-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-011-0875-z

Keywords

Search

Navigation