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Experimental reduction of nestling hemoglobin concentration in combination with ectoparasite load manipulation affects nestling morphology and begging behavior, but not adult behavior

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Abstract

Young nest-bound birds often face a diversity of ectoparasites that typically feed on blood and can negatively affect nestling morphological and physiological traits, including hemoglobin concentration. While hemoglobin concentration can be correlated with nestling performance, such as body mass, it is unknown whether variation in hemoglobin is the direct proximate factor responsible for variation in morphology, or if nestling traits simply co-vary with hemoglobin concentration due to a number of similar factors influencing both traits. If hemoglobin concentration does directly influence the phenotype of nestlings, then the reduction in nestling hemoglobin concentration by ectoparasites may cause other negative effects commonly associated with parasitism. By experimentally reducing the hemoglobin concentration of nestling Tree Swallows (Tachycineta bicolor) using phenylhydrazine hydrochloride (PHZ), we tested whether reduced hemoglobin concentration could be the mechanism that causes changes in nestling morphology and behavior in response to increased parasitism. Parasite loads were manipulated in conjunction with the PHZ treatment. Nestlings injected with PHZ displayed no change in hemoglobin concentration 2 days post-injection, whereas control nestlings showed the typical increase that occurs during early development. By 6 days post-injection, the parasite, but not PHZ, treatment significantly affected hemoglobin concentration. Both treatments interacted to affect begging intensity, while size and growth rate of nestlings were only affected by the parasite load manipulation. This study demonstrates the potential use of PHZ in nestlings to tease apart the effects of parasitism and reduced hemoglobin, but the results suggest incorporating a second injection of PHZ to better replicate the pattern of hemoglobin reduction created by hematophagous ectoparasites.

Zusammenfassung

Experimentelle Reduzierung der Hämoglobinkonzentration bei Nestlingen in Kombination mit Manipulation der Ektoparasitenlast beeinflusst Morphologie und Bettelverhalten der Nestlinge jedoch nicht das Verhalten der Altvögel.

Nesthocker sind häufig einer Vielfalt an Ektoparasiten ausgesetzt, die sich typischerweise vom Blut ernähren und die morphologischen und physiologischen Eigenschaften der Nestlinge einschließlich der Hämoglobinkonzentration negativ beeinflussen können. Die Hämoglobinkonzentration kann mit der Nestlingsentwicklung, wie z. B. mit der Körpermasse, korrelieren. Jedoch ist unbekannt, inwiefern die Unterschiede im Hämoglobingehalt als direkter, unmittelbarer Faktor für die Variation in der Morphologie verantwortlich sind, oder ob aufgrund ähnlicher Faktoren sowohl die Eigenschaften der Nestlinge also auch die der Hämoglobinkonzentration beeinflusst werden und diese somit miteinander kovariieren. Falls die Hämoglobinkonzentration den Phänotyp der Nestlinge direkt beeinflussen würde, dann riefe die durch eine Ektoparasitenlast reduzierte Hämoglobinkonzentration der Nestlinge möglicherweise weitere typische negative parasitäre Effekte hervor. Durch eine experimentell reduzierte Hämoglobinkonzentration bei Nestlingen der Sumpfschwalbe (Tachycineta bicolor) mittels Phenylhydrazinhydrochlorid (PHZ) haben wir getestet, ob eine reduzierte Hämoglobinkonzentration der verantwortliche Mechanismus für die Veränderungen in Nestlingsmorphologie und –verhalten darstellen könnte, als Reaktion auf einen erhöhten Parasitismus. Die Parasitenlast wurde in Verbindung mit der PHZ-Behandlung manipuliert. Nestlinge, welche PHZ injiziert bekommen hatten, zeigten zwei Tage nach der Injektion keine Veränderung in der Hämoglobinkonzentration, wohingegen Nestlinge der Kontrollgruppe eine für die frühe Entwicklungsphase typische Erhöhung der Konzentration zeigten. Sechs Tage nach der Injektion beeinflusste die Parasitenlast, jedoch nicht die PHZ-Behandlung, die Hämoglobinkonzentration signifikant. Beide Behandlungen zusammen beeinflussten das Bettelverhalten, während Größe und Wachstumsrate der Nestlinge nur durch die Manipulation der Parasitenlast beeinflusst wurden. Wir demonstrieren hier die potentielle Anwendung von PHZ bei Nestlingen, um die Auswirkungen durch die Parasiten und denen des reduzierten Hämoglobins zu trennen. Jedoch raten wir dazu, eine zweite PHZ-Injektion einzubeziehen, um das durch hämatophage Ektoparasiten hervorgerufene Muster der Hämoglobinreduzierung besser zu replizieren.

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Acknowledgements

We thank J. Bisaro, S. Sparks, and K. Sweet for assistance in the field and the City of Prince George for granting us access to their property. Comments by two anonymous referees improved a previous version of the manuscript.

Funding

Funding was provided by the Natural Sciences and Engineering Research Council of Canada through a Discovery Grant to RDD and an Alexander Graham Bell Canada Graduate Scholarship to IAG. Additional funding was provided by the University of Northern British Columbia, Canada Foundation for Innovation, and the British Columbia Knowledge Development Fund. None of the funders had any input into the content of the manuscript, nor required approval of the manuscript prior to the submission.

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Author notes

  1. Ilsa A. Griebel

    Present address: Centre for Conservation Research, Calgary Zoological Society, 1300 Zoo Road NE, Calgary, AB, T2E 7V6, Canada

Authors and Affiliations

  1. Ecosystem Science and Management Program, University of Northern British Columbia, 3333 University Way, Prince George, BC, V2N 4Z9, Canada

    Ilsa A. Griebel & Russell D. Dawson

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  1. Ilsa A. Griebel
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  2. Russell D. Dawson
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Correspondence to Ilsa A. Griebel.

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The authors declare they have no competing interests.

Ethical approval

This study complies with the current laws of Canada. The University of Northern British Columbia Animal Care and Use Committee on behalf of the Canadian Council on Animal Care approved our research protocols. All procedures performed were in accordance with the ethical standards of the institution at which the study was conducted.

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Communicated by C. G. Guglielmo.

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Griebel, I.A., Dawson, R.D. Experimental reduction of nestling hemoglobin concentration in combination with ectoparasite load manipulation affects nestling morphology and begging behavior, but not adult behavior. J Ornithol 161, 35–45 (2020). https://doi.org/10.1007/s10336-019-01706-2

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