Punekar, I R.
Bio 3255
Critique- Sparrows
2/18/2016
Seasonal Variations in Levels of Immune System Response in Latitudinally-separated
Populations of House Sparrows adaptions to Parasite Prevalence and Reproductive Life History
Changes.
House sparrows in tropical climates face different challenges and enjoy different benefits
than those in temperate climates. This can result in intraspecific phenotypic variation. In order
to ascertain whether a variant feature is genetically or environmentally determined, a commongarden experiment can be conducted. A common garden experiment involves the raising
members of at least two phenotypically divergent populations in a single environment. If the
expression of the feature is environmentally determined, the two specimens will exhibit the same
phenotype. If it is genetically determined, the phenotype will differ, and if, as is often the case,
the trait is determined by a combination of environmental and genetic factors, the type and level
of change observed is indicative of the plasticity of that trait. Such phenotypic variation can lead
to divergence between species (Ricklefs 2001: 201). A group of researchers led by Dr. Lynn
Martin II at Princeton University, NJ, recently conducted a study on intraspecific seasonal
variations in immune function in Neotropical and north-temperate populations of house sparrow
(Passer domesticus). Martin et al. used both wild birds as well as common-garden reared birds
to determine the nature of the variation. In the experiment, immune activity was elicited using
PHA (phytohemagglutinin), a commonly used benign plant-based mitogen known to induce a
cell-mediated immune response. One of the advantages of using PHA is that, unlike an active
virus, its effects can confidently be attributed to immune response only and not to any
pathological effect. Furthermore, the direct effects of this exposure are limited to the blood and
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immune system (Martin et al. 2003). The experimenters found that seasonal variations of
immune activity are higher in wild north-temperate (New Jersey) house sparrows than in wild
Neotropical (Panamian) sparrows; the New Jersey birds had higher levels of immune activity
than the Panamian birds during the late and non-breeding seasons and lower levels during the
early breeding season. Under a common garden setting, similar variations occurred, although the
length of captivity had the same effect of first decreasing then increasing immune activity in both
populations (Martin et al. 2004).
In this paper, I will summarize the results and methods of the study by Martin et al., and
to describe how their results contribute to what is generally known about the immune system in
birds, as well as the concepts of intraspecific phenotypic variation, life history ecology, parasitehost interactions and trade-offs.
According to unpublished work by Martin et al., the incidence of blood parasites varies
between the two populations. Blood parasites are a threat to Neotropical sparrows throughout
the year, whereas they are more so for north-temperate sparrows during the late breeding season
and undetectable during the non-breeding season. Birds in tropical environments also tend to
have a greater risk of parasite infection. Therefore, Neotropical sparrows should exhibit high
immune responses during the late breeding season, low levels of response during the nonbreeding season greater immune responses (Lindstrom et al. 2004). The aim of this study was to
determine whether these hypotheses were true, that is, whether immune response is latitudinally
dependent (Martin et al. 2004). Martin et al. expected the wild birds to exhibit latitudinal
variation in immune activity in correlation to the differing levels of parasite threat in the two
climates. However, this relationship is complicated by the fact that reproduction is also a very
demanding process, both energetically as well as nutritionally, and, since both immune responses
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and reproduction cannot be maximized, there must exist a trade-off which takes into account
both the limit of resources as well as the environmental adaptation to parasite infection
(Bonneaud et al. 2003, Martin et al. 2003, Ricklefs 2001:210, 338).
Many Neotropical passerines have smaller clutches but longer breeding seasons, as well
as longer embryonic development times and higher survival rates than Temperate passerines
(reviewed by Martin et al. 2004). These differences have been observed between different
species as well as within different populations of the same species- a fact that suggests direct
involvement of environmental variables such as food availability and predation, and, as Martin et
al. hypothesize, immune stressors which can lead to significant trade-offs between the immune
and reproductive systems. House sparrows follow this trend in that north-temperate birds tend to
have temporally concentrated, larger clutch sizes because of the short window of favorable
weather. Tropical sparrows, on the other hand, which enjoy a steadier climate conducive to
reproduction, tend to lay smaller clutches that are distributed throughout their (much longer)
breeding season. Martin et al. split the year into three road seasons: the early-breeding season
(Mar – April), the late-breeding season (Jul – Aug), and the non-breeding season (Oct – Nov).
The actual breeding seasons, however, of the two populations differ as follows: tropical house
sparrows tend to reproduce from January to August (early and late seasons) whereas temperate
birds typically breed only during the months between April and August (Martin et al. 2004).
The experimenters tested immune activity in birds from both locations in the following
settings: wild, 5 months captivity, and 18 months captivity. The Neotropical house sparrows
were captured in Colon, Panama, while the north-temperate House Sparrows were captured in
Princeton, New Jersey. There is a difference of about 31˚ of latitude between the two locations.
The birds were stressed according to a phytohemagglutinin wing web technique on the left wing
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(Martin et al. 2003), and immune responses measured by the size of resultant wing web
swellings after 24 h. The birds were all caught using mist nets, their sexes identified by
plumage, banded, measured by tarsus length, and then segregated according to age as either
adults or juveniles. The birds were well fed and appeared to take be eating well. For the wild
trials, the birds were held for no more than 24 hours before being given the PHA challenge
(Martin et al. 2004).
New Jersey temperate house sparrows showed significant seasonal variation in immune
response, while house sparrows obtained from Panama exhibited seasonal variation to much
lesser degree. New Jersey birds had the highest immune response levels outside their normal
(early) breeding season, when parasite prevalence is highest. However, immune response during
the non-breeding season, when parasite prevalence is minimal and immune response was
expected to drop, was also high (within 10% of the late-breeding season levels). Parasite
prevalence is intermediate during the early breeding season, when the north-temperate sparrows
exhibited very low levels of immune response (less than 25% of late-breeding season levels).
The Panamanian birds showed much more stable immune response levels, with response levels
during all three seasons being relatively close, with only slight elevations during the early
breeding season. Response levels in Neotropical sparrows were also, except in the early
breeding season when north-temperate response levels were very low, lower than those of northtemperate birds (Martin et al. 2004).
These results mostly contradict those expected in light of variations in blood parasite
prevalence in that, if immune response is dependant on parasite presence alone, Panama birds,
which face greater risk to parasites, ought to exhibit consistently higher immune activity. Also,
while New Jersey birds did show the highest levels of immune activity during the period of
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highest parasite threat, the late breeding season, the predictions made about the other seasons
were not validated. These data can be explained by the interactions of, and trade-offs between
immune function and reproduction. Both are highly demanding tasks in terms of energetics and
nutrition and Martin et al. conclude that one good must be traded-off in order for the bird to
pursue the other. Due to the fact that temperate bird species are limited to only a few months of
prime breeding time, they are forced to focus their reproductive efforts into a few (2-3) larger
clutches, unlike the tropical birds which tend to have (4 or more) smaller clutches. Reproduction
during the early breeding season therefore takes priority over immune response because it is vital
to the continuation of the species and can only occur during that time. The constancy of immune
activity in the Neotropical sparrows is in line with the findings that parasite threat is constant and
reproduction more spaced out in tropical birds. The fact that immune responses were lower than
expected, considering the higher risk from parasites in the tropics, only supports the idea of there
being a delicate trade-off between resource allocation to the immune system or reproduction;
Panamanian birds do not experience the sort of intense divestiture of immunocompetence seen in
the early breeding season of north-temperate birds, but experience a smaller though prolonged
trade-off with reproductive ability (Martin et al. 2004).
Testing during the second half, the common-garden portion, of the experiment was
identical to that of the first, although only non-breeding sparrows were examined in order to
prevent complications arising from differences in reproductive patterns. The birds were kept in
two separate facilities, which were newly built and designed to minimize interference by the
experimenters. The buildings were layered with sand which would permit less frequent cleaning,
and the researchers made sure to disturb the birds for no more than 30min at a time. The
temperature and other environmental settings mimicked those of the New Jersey environment in
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one facility and the Panamanian environment in the other. The photoperiod was maintained at
New Jersey standards in both because of indications that New Jersey birds would not engage in
normal reproduction otherwise (Martin et al. 2004).
The data obtained from this portion of the experiment showed, surprisingly, that captivity
time, independent of all other variables, affected the immune responses recorded. After 5
months, immune responses in all the birds, regardless of origin and common-garden setting,
dropped to levels much less than those measured in the wild (more than half in some cases).
After 11 months, however, the immune responses actually increased in all birds to levels above
those obtained in the wild. These data were correlated with similar changes in weight of the
birds. Martin et al. were unable to explain this since all the birds appeared to be eating well
(Martin et al. 2004). However, the fact that most birds lost weight by 5 mo, but gained weight
after 18 mo, is possibly due to the stresses involved in captivity, and the subsequent acclimation
to those stresses. The data also showed that after 5 mo, latitudinal differences in immune
response were insignificant, however, those differences were restored to levels seen in the wild
after 18 mo. Martin et al. ascribe these strange findings to the fact that, after 5 mo, all of the
birds had lost weight and exhibited immune responses so low that they confounded the
measurement of the differences between populations. They also, rather weakly, conclude that
their study suggests that latitudinal variation in levels of immune system response is more than
simply the results of environmental acclimation.
Martin et al.’s study supports common notions of environmental adaptation and the need
for critical trade-offs between immune function and other important biological investments such
as reproduction and growth in birds. The experiment also clearly shows that levels and
variations of immune activity in are latitudinally determined, however, does not offer any
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experimental data addressing why or how. A previous paper published by Martin et al. in 2003,
describes the analysis and quantification of the costs of an immune response to PHA as
compared to reproduction (a PHA wing web response costs 4.20kJ/day, or about half an egg)
(Martin et al. 2003). This more recent paper also does not cite adequate evidence or make a
convincing argument regarding the plasticity of immune function. These insufficiencies are
primarily due to drawbacks, omissions, and uncontrolled variables in the experimental design,
which will be dealt with shortly. As a result, this experiment contributes little to the
advancement of our understanding of phenotypic plasticity and life history changes.
Nonetheless, the study is valuable in that it presents solid empirical evidence for the presence of
intraspecific phenotypic variation. It also addresses immunocompetence trade-offs in birds, a
topic which lacks in depth exploration. This experiment serves to establish some much-needed
groundwork in the field, and raises many questions which need to be answered. For instance,
what exactly is the nature of the trade-off between immunocompetence and reproduction? How
plastic is immunocompetence, and how much is that trait influenced by genetic and
environmental variation? Working backwards, can immune stressors lead to decreased
performance in reproductive ability and other metabolically taxing ventures? These are some of
the issues touched on but ultimately left unanswered by Martin et al.
Some of the many criticisms I had of the experiment include the capturing and
maintenance of the birds, in particular the Panamanian ones, as well as the conditions under
which all the birds were held during the common garden portion of the study. The Panamanian
birds were captured in late July 2001, but were not brought to the quarantine facility in New
Jersey until October 2001 for logistical reasons, until which they were kept in a rooftop aviary
and fed a diet of finch seed mix, vitamin supplements, water, and boiled, mashed chicken eggs.
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It is important to note, however, that this diet is not the typical diet for the Panamanian House
Sparrow, although Martin et al. did not address this fact at all. It is conceivable that dietary
supplements included in the artificial diet play an immunosuppressive or immostimulatory role
(Latshaw 1991, Moore et al. 2003). Since both House Sparrows were given this diet for different
amounts of time, it arises as an uncontrolled variable which may have influenced the levels of
immune response, especially considering the fact that weight change 24hrs post-immune
response was used as a dependent variable. Furthermore, the paper does not describe the rooftop
aviary environment, or even make the claim that it is equivalent to a natural habitat. This is also
important, especially in light of the results which indicate that the length of captivity was one of
the only factors related to changes in immune response levels in the common-garden aspect of
the experiment. The common garden experiment was also lacking, I felt, in the sole use of the
New Jersey photoperiod, a variable which Martin et al. acknowledge may have had uncontrolled
effects on their results. There was also a lack of testing in reciprocal environments, which was
problematic, because, whereas the conditions tested of both sets of birds may have been the
same, the deviances from natural settings were certainly not, which may have led to particular
stresses on the tropical birds which were not present for the neo-Temperate ones.
Martin et al.’s study, for the most part, supports previous knowledge on the subject, and
despite the fact that I still find the study very informative and useful, there is admittedly little in
the way of surprise or groundbreaking discovery involved. Ricklef’s characterization of life
history changes and intraspecific phenotypic variation was reinforced. Furthermore, the
execution and results of the common-garden test were almost prototypical, showing a clear effect
of environment as well as a lesser, ingrained effect due perhaps to genetic variation, much like
the example of Nebraska lizards given in The Economy of Nature (203-205). Another idea
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presented that is supported is that parasite prevalence would, via prolonged parasite-host
interactions, selectively result in a correlated host defense mechanism. However, this was only
shown effectively in the Panama sparrows. The results from the New Jersey birds directly reflect
Ricklef’s discussion of the trade-off between fecundity vs. survival, which argues that, in cases
where mortality is high, due to threats like parasites, selection favors increased investment in
reproduction over survival (immunocompetence). In fact, the small temporal window for
reproductive success in north-temperate birds is what leads to the heavy divestiture of resources
from immunocompetence to reproduction, which, in an almost semelparous manner, allows the
birds to produce larger clutches and devote more energy towards reproduction at the cost of
decreasing chances of survival.
I found this study to contribute considerably to addressing the concepts and ecological
issues of trade-offs, intraspecific phenotypic variation, life history ecology, as well as parasitehost interactions. This is especially true when one considers the dearth of knowledge on the
immune system in undomesticated birds. However, it is clear that the depth of this research is
not adequate enough to make it a foundational or illuminating piece. Nonetheless, studies which
follow up on this research may be able to significantly advance our understanding of
immuncompetence and its trade-offs in avian species.
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Literature Cited
Martin, L. B. 2nd, M. Pless, J. Svoboda, and M. Wikelski. 2004. Immune activity in temperate
and tropical house sparrows: a common-garden experiment. Ecology 85: 2323-2331.
Ricklefs, R. E. 2001. The Economy of Nature (fifth edition). W. H. Freeman, New York, New
York, USA.
Martin, L. B. 2nd, A. Scheuerlein, and M. Wikelski. 2003. Immune activity elevates energy
expenditure of house sparrows: link between direct and indirect costs? Proceedings of
the Royal Society of London. Series B. Biological sciences 270: 153-158.
Lindstrom, K.M., J. Foufopoulos, H. Parn, and M. Wikelski. 2004. Immunological investments
reflect parasite abundance in island populations of Darwin’s finches. Proceedings of the
Royal Society of London. Series B. Biological sciences 271: 1513-1519.
Bonneaud, C., J. Mazuc, G. Gonzalez, C. Haussy, O. Chastel, B. Faivre, and G. Soros. 2003.
Assessing the cost of mounting an immune response. The American Naturalist 161:367379
Latshaw, J.D. 1991. Nutrition—mechanisms of immunosuppresssion. Veterinary immunology
and immunopathology 30: 111-120.
Moore, C.B., and T.D. Siopes. 2003. Melatonin enhances cellular and humoral immune
responses in the Japanese quail (Coturnix coturnix japonica) via an opiatergic
mechanism. General and Comparative Endocrinology 131: 258-263.