Functional
Ecology 2005
19, 1001–1007
© 2005 British
Ecological Society
1001
Blackwell Publishing, Ltd.
Increase in the constitutive innate humoral immune system
in Leach’s Storm-Petrel (Oceanodroma leucorhoa) chicks
is negatively correlated with growth rate
R. A. MAUCK,*† K. D. MATSON,‡ J. PHILIPSBORN* and R. E. RICKLEFS‡
*Biology Department, Kenyon College, Gambier, OH 43022, USA, and ‡Department of Biology, University of
Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis, MO 63121–4499, USA
Summary
1. Using a simple technique for assessing constitutive innate immune function recently
adapted for use in wild populations, we characterize changes in avian immune system
development by repeated measurements of individuals over the period of nestling growth
in a wild population of Leach’s Storm-Petrels (Oceanodroma leucorhoa).
2. We measured levels of natural antibodies (NAb) during the early, middle and late
phases of storm-petrel development and related these levels and NAb rate of change
to mass and wing length growth. We used natural variation in nestling growth to assess
the influence of nutritional status on the development of innate immunity.
3. NAb levels increased over the first 50 days of chick development; however, rate of
increase was inversely proportional to wing growth.
4. Initial titre levels were inversely proportional to rate of change in NAb levels over
the first 50 days of immune development. This suggests that individuals with low initial
NAb levels accelerate immune development to reach adult levels, whereas individuals
with high initial levels do not.
5. As in previous studies, our results demonstrate an inverse relationship between
growth rate and development of components of the avian immune system. While such
a relationship is consistent with the idea that immune function development involves
trade-offs, the processes involved are more complex than simple energy allocation.
Key-words: Development, innate humoral immune system, natural antibodies, seabirds, nestling
Functional Ecology (2005) 19, 1001–1007
doi: 10.1111/j.1365-2435.2005.01060.x
Introduction
Immune function is increasingly seen in the context of
life-history trade-offs (Sheldon & Verhulst 1996; Norris
& Evans 2000; Martin et al . 2001; Tella, Scheuerlein
& Ricklefs 2002; Schmid-Hempel 2003). The ability to
respond effectively to parasites and pathogens has been
shown to have fitness benefits in terms of body condition,
survival and reproductive success (e.g. Horak et al .
1999; Johnsen et al . 2000; Alonso-Alvarez & Tella 2001;
Christe et al . 2001; Svensson, Sinervo & Comendant
2001; Råberg & Stjernman 2003). With benefits come
costs; resources allocated to the immune system are
not available for other functions. For example, experi-
mentally elicited immune responses have been shown
to decrease avian nestling growth (Fair, Hansen &
Ricklefs 1999; Alonso-Alvarez & Tella 2001; Whitaker
& Fair 2002; Nilsson 2003; Soler et al . 2003; Brommer
2004a), degrade adult body condition (Alonso-Alvarez
& Tella 2001; Sanz et al . 2004) and increase metabolic
rate (Ots et al . 2001).
Many studies (reviewed in Tella et al . 2002) have
employed the phytohaemagglutinin (PHA) skin test to
assess non-specific cellular immunity (commonly referred
to as cell-mediated immunity, or CMI). Although the
PHA response involves proliferation of T cells, PHA
also attracts other immune cells, including basophils
and heterophils, to the injection site and causes inflam-
mation (Smits, Bortolotti & Tella 1999). Response to
PHA is typically positively correlated with nestling
body condition or food availability, sometimes mediated
through an effect of brood size or season (e.g. Merino,
Moller & de Lope 2000; Dubiec & Cichon 2001;
Hoi-Leitner et al . 2001; Westneat et al . 2004).
Much recent work on immune function in develop-
ing birds has focused on measuring induced immuno-
logical responses, a subset of immune function that
involves adaptive humoral immunity (e.g. antibody
responses to specific antigens) and cellular immunity
†Author to whom correspondence should be addressed.
E-mail: mauckr@kenyon.edu