Skip to main content
Log in

Aggression, body condition, and seasonal changes in sex-steroids in four hummingbird species

  • Original Article
  • Published:
Journal of Ornithology Aims and scope Submit manuscript

Abstract

Hummingbirds present a unique combination between extremely high life costs and a number of efficient adaptations to fuel these demands. In addition to cognitive abilities, territorial hummingbirds display aggressive behaviors that allow for access to better food resources. In year-round territorial species, male–male territorial aggression is similar between breeding and non-breeding seasons; however, the endocrine mechanisms underlying control of territoriality during these distinct seasonal periods may differ. In many species, testosterone (T) triggers increased aggression during the breeding season whereas territoriality in the non-breeding season can be regulated by circulating the biologically inert sex steroid precursor dehydroepiandrosterone (DHEA) and converting it to T in target tissues. The seasonal hormonal regulation of hummingbird territorial behavior has heretofore been unknown. Our goal was to assess seasonal changes in sex steroids, territorial aggression levels, and body condition during reproductive and non-reproductive seasons in hummingbirds. To validate the use of cloacal fluid (CF) for the study of sex steroids, steroid levels in plasma and CF were correlated in Sephanoides sephaniodes. During the reproductive season, Calypte. anna, Archilochus alexandri, and Selasphorus rufus males showed high levels of T that were positively correlated with aggression, but the relationship between T and body condition was not consistent across species. As expected, T levels in females were significantly lower than in males in all seasons, however still detectable. During the non-reproductive season, CF DHEA of Calypte anna was high and positively correlated with aggressive behaviors and body condition. Our results suggest that hummingbirds display aggressive behaviors that could be linked to different hormones during the breeding and non-breeding seasons.

Zusammenfassung

Aggressionsverhalten, Körperkondition und jahreszeitliche Schwankungen der Sexualsteroidspiegel bei vier Kolibriarten

Kolibris verbinden in einzigartiger Weise eine extrem kostspielige Lebensweise mit einer Reihe von Anpassungsleistungen, um ihren Energiebedarf effizient zu decken. Zusätzlich zu ihren kognitiven Fähigkeiten verfügen territoriale Kolibris über aggressive Verhaltensweisen, die ihnen den Zugang zu besseren Nahrungsquellen sichern. Bei Arten, die ganzjährig Reviere verteidigen, ist die territoriale Aggression zwischen Männchen zur Brutzeit ähnlich wie außerhalb; allerdings können sich die der Steuerung der Territorialität zugrunde liegenden endokrinen Mechanismen während dieser jahreszeitlich klar getrennten Zeiträume unterscheiden. Bei vielen Arten löst Testosteron (T) eine Zunahme des Aggressionsverhaltens während der Brutsaison aus, wohingegen die Territorialität außerhalb der Brutzeit durch den Einsatz des biologisch inerten Sexualsteroid-Vorläufers Dehydroepiandrosteron (DHEA) reguliert werden kann, welcher dann im Zielgewebe in T umgewandelt wird. Die jahreszeitliche hormonelle Steuerung des Territorialverhaltens bei Kolibris war bislang unbekannt. Unser Ziel war es, jahreszeitliche Schwankungen des Spiegels von Sexualsteroiden, das Ausmaß territorialer Aggression sowie die Körperkondition der Kolibris jeweils während und außerhalb der Fortpflanzungszeit zu ermitteln. Um die Eignung der Kloakenflüssigkeit (cloacal fluid, CF) für die Untersuchung von Sexualsteroiden zu testen, wurden bei Sephanoides sephaniodes die jeweiligen Steroidspiegel in Plasma und CF miteinander in Bezug gesetzt. Während der Fortpflanzungsperiode zeigten Männchen von C. anna, Archilochus alexandri und Selasphorus rufus jeweils hohe T-Spiegel, welche positiv mit dem Aggressionsverhalten korrelierten; das Verhältnis zwischen T und der Körperkondition stimmte jedoch nicht bei allen Arten überein. Erwartungsgemäß lagen die T-Spiegel bei den Weibchen zu allen Jahreszeiten signifikant niedriger als bei den Männchen, waren aber trotzdem nachweislich vorhanden. Außerhalb der Fortpflanzungszeit lag der CF-Wert für DHEA bei Calypte anna hoch und korrelierte positiv mit dem Aggressionsverhalten und der Körperkondition. Unsere Ergebnisse legen nahe, dass die von Kolibris gezeigten aggressiven Verhaltensweisen zur Brutzeit beziehungsweise außerhalb dieser an verschiedene Hormone gekoppelt sein könnten.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Armstrong LE (2005) Hydration assessment techniques. Nutr Rev 63:S40–S54

    Article  PubMed  Google Scholar 

  • Brenowitz EA, Arnold AP (1993) Hormone accumulation in song regions of the canary brain. J Neurobiol 23:871–880

    Article  Google Scholar 

  • Byers J, Hebets E, Podos J (2011) Female mate choice based upon male motorperformance. An Behav 79:771–778

    Article  Google Scholar 

  • Camfield AF (2006) Resource value affects territorial defense by broad tailed and rufous hummingbirds. J Field Ornithol 77:120–125

    Article  Google Scholar 

  • Copenhaver C, Ewald PW (1980) Cost of territory establishment in hummingbirds. Oecologia 46:155–160

    Article  PubMed  Google Scholar 

  • Elekonich MM, Wingfield JC (2000) Seasonality and hormonal control of territorial aggression in female song sparrows (Passeriformes: Emberizidae: Melospiza melodia). Ethology 106:493–510

    Article  Google Scholar 

  • Gomez Y, Velazquez PN, Peralta-Delgado I, Mendez MC, Vilchis F, Juarez-Oropeza M, Pedernera E (2001) Follicle stimulating hormone regulates steroidogenic enzymes in cultured cells of the chick embryo ovary. Gen Comp Endoc 121:305–315

    Article  CAS  Google Scholar 

  • González-Gómez PL, Estades CF (2009) Is natural selection promoting sexual dimorphism in the Green-backed firecrown hummingbird (Sephanoides sephaniodes)? J Ornithol 150:351–356

    Article  Google Scholar 

  • González-Gómez PL, Vasquez R (2006) A field study of spatial memory in Sephanoides sephaniodes. Ethology 112:790–795

    Article  Google Scholar 

  • González-Gomez PL, Ricote-Martínez N, Razeto-Barry P, Bozinovic F (2011) Thermoregulatory cost affects territorial behavior in hummingbirds: a model and its application. Behav Ecol Sociobiol 65:2141–2148

    Article  Google Scholar 

  • González-Gómez PL, Bozinovic F, Vásquez RA (2011a) Elements of episodic-like memory in free-living hummingbirds, energetic consequences. An Behav 81:1257–1262

    Article  Google Scholar 

  • González-Gómez PL, Vásquez RA, Bozinovic F (2011b) Flexibility of foraging behavior in hummingbirds: the role of energy constraints and cognitive abilities. Auk 128:36–42

    Article  Google Scholar 

  • Goyman W (2005) Noninvasive monitoring of hormones in bird droppings physiological validation, sampling, extraction, sex differences, and the influence of diet on hormone metabolite levels. Ann NY Acad Sci 1046:35–53

    Article  CAS  Google Scholar 

  • Goymann W, Landys MM, Wingfield JC (2007) Distinguishing seasonal androgen responses from male–male androgen responsiveness—revisiting the challenge hypothesis. Horm Behav 51:463–476

    Article  CAS  PubMed  Google Scholar 

  • Hainsworth FR (1978) Feeding: models of costs and benefits in energy regulation. Am Zool 18:701–714

    Article  Google Scholar 

  • Hau M (2007) Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories. Bioessays 29:133–144

    Article  CAS  PubMed  Google Scholar 

  • Hau M, Wikelski M, Soma KK, Wingfield JC (2000) Testosterone and year-round territoriality in a tropical bird. Gen Comp Endoc 117:20–33

    Article  CAS  Google Scholar 

  • Hiebert SM, Ramenofsky M, Salvante K, Wingfield JC, Gass CL (2000) Noninvasive methods for measuring and manipulating corticosterone in hummingbirds. Gen Comp Endoc 120:235–247

    Article  CAS  Google Scholar 

  • Ketterson ED, Nolan V Jr, Sandell M (2005) Testosterone in females: mediator of adaptive traits, constraint on the evolution of sexual dimorphism, or both? Am Nat 166:S85–S98

    Article  PubMed  Google Scholar 

  • Kodric-Brown A, Brown JH (1978) Influence of economics, interspecific competition, and sexual dimorphism on territoriality of migrant rufous hummingbirds. Ecology 59:285–296

    Article  Google Scholar 

  • López-Calleja MV, Bozinovic F (2003) Dynamic energy and time budgets in hummingbirds: a study in Sephanoides sephaniodes. J Comp Biochem Physiol A 134:283–295

    Article  Google Scholar 

  • McGlothlin JW, Jawor JM, Ketterson ED (2007) Natural variation in a testosterone-mediated trade-off between mating effort and parental effort. Am Nat 170:864–875

    Article  PubMed  Google Scholar 

  • Müller W, Eising C, Dijkstra C, Groothuis T, Sageder G (2002) Sex differences in yolk hormones depend on maternal social status in leghorn chickens (Gallus gallus domesticus). Proc R Soc Lon B 269:2249–2255

    Article  CAS  Google Scholar 

  • Norton ME, Arcese P, Ewald PW (1982) Effect of intrusion pressure on territory size in black-chinned hummingbirds (Archilochus-alexandri). Auk 99:761–764

    Google Scholar 

  • Ogawa S, Lubahn D, Korach K, Pfaff D (1997) Behavioral effects of oestrogen receptor gene distribution in male mice. Proc Natl Acad Sci USA 94:1476–1481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pärn H, Lindström KM, Sandell M, Amundsen T (2008) Female aggressive response and hormonal correlates—an intrusion experiment in a free-living passerine. Behav Ecol Sociobiol 62:1665–1677

    Article  Google Scholar 

  • Schleussner G, Dittami JP, Gwinner E (1985) Testosterone implants affect molt in male European Starlings, Sturnus vulgaris. Physiol Zool 58:597–604

    Article  Google Scholar 

  • Soma KK, Wingfield JC (2001) Dehydroepiandrosterone in song plasma: seasonal regulation and relationship to territorial aggression. Gen Comp Endoc 123:144–155

    Article  CAS  Google Scholar 

  • Soma KK, Traimontin AD, Wingfield JC (2000) Oestrogen regulates male aggression in the non-breeding season. Proc Roy Soc Lon B 267:1089–1096

    Article  CAS  Google Scholar 

  • Soma KK, Wissman AM, Brenowitz EA, Wingfield JC (2002) Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird. Horm Behav 41:203–212

    Article  CAS  PubMed  Google Scholar 

  • Stiles FG (1971) Time, energy, and territoriality of the anna hummingbird (Calypte anna). Science 173:818–820

    Article  CAS  PubMed  Google Scholar 

  • Suarez RK (1992) Hummingbird flight: sustaining the highest mass-specific metabolic rates among vertebrates. Experientia 48:565–570

    Article  CAS  PubMed  Google Scholar 

  • Suarez RK, Gass CL (2002) Hummingbird foraging and the relation between bioenergetics and behaviour. Comp Biochem Physiol A 133:335–343

    Article  Google Scholar 

  • Temeles EJ, Goldman RS, Kudla AU (2005) Foraging and territory economics of sexually dimorphic purple-throated caribs (Eulampis jugularis) on three heliconia morphs. Auk 122:187–204

    Article  Google Scholar 

  • Wasser SK, Thomas R, Nair PP, Guidry C, Southers J, Lucas J, Wildt DE, Monfort SL (1993) Effects of dietary fiber on faecal steroid measurements in baboons (Papio cynocephalus cynocephalus). J Rep Fertil 97:569–574

    Article  CAS  Google Scholar 

  • Wingfield JC (1984) Androgens and mating systems: testosterone-induced polygyny in normally monogamous birds. Auk 101:665–671

    Article  Google Scholar 

  • Wingfield JC, Soma KK (2002) Spring and autumn in song sparrows: same behavior, different mechanisms? Integr Comp Biol 42:11–20

    Article  PubMed  Google Scholar 

  • Wingfield JC, Henger RE, Dufty AM Jr, Ball GF (1990) The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846

    Article  Google Scholar 

  • Wingfield JC, Vleck CM, Moore MC (1992) Seasonal changes of the adrenocortical response to stress in birds of the sonoran desert. J Exp Zool 264:419–428

    Article  CAS  PubMed  Google Scholar 

  • Wingfield JC, Lynn S, Soma KK (2001) Avoiding the ‘costs’ of testosterone: ecological bases of hormone–behavior interactions. Brain Beh Evol 57:239–251

    Article  CAS  Google Scholar 

  • Yu JYL, Marquardt RR (1973) Synergism of testosterone and estradiol in the development and function of the magnum from the immature chicken oviduct. Endocrinology 92:563–572

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This paper is dedicated to the memory of Loreto Godoy. We thank Baggins End Community, and Lee James of Tierra Verde Vegetables for allowing us to work in their properties. We thank Kara Sweeney and Holly Ernest for contacts and sampling help. This research was supported by CONICYT, Postdoc Becas Chile to PGG and the Endowed Professorship in Physiology to JCW, College of Biological Sciences, University of California, Davis and Grant Number IOS-0750540 from the National Science. Foundation to JCW.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paulina L. González-Gómez.

Additional information

Communicated by L. Fusani.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González-Gómez, P.L., Blakeslee, W.S., Razeto-Barry, P. et al. Aggression, body condition, and seasonal changes in sex-steroids in four hummingbird species. J Ornithol 155, 1017–1025 (2014). https://doi.org/10.1007/s10336-014-1088-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10336-014-1088-y

Keywords

Navigation