In this contribution I present an extended but testable hypothesis (or “evolutionary scenario”) to explain how and why many life-history features of latitudinal migrant shorebirds, basically characterised by the correlation between habitat choice in the winter and the breeding season, may be functionally and causally intertwined. The most novel (and contentious) aspect of the hypothesis is that historical restrictions in suitable habitat may generate further restriction of suitable habitat with the causal chain consisting of population bottlenecks, leading to reduced adaptive genetic variation, leading to reduced ability to fight diseases, thus affecting potential habitat choice.

Piersma, Theunis,

English

Piersma, Theunis

University of Groningen Research Database

“Coastal” versus “inland” shorebird species:interlinked fundamental dichotomies between their life- and demographic histories?

In this contribution I present an extended but testable hypothesis (or “evolutionary scenario”) to explain how and why many life-history features of latitudinal migrant shorebirds, basically characterised by the correlation between habitat choice in the winter and the breeding season, may be functionally and causally intertwined. The most novel (and contentious) aspect of the hypothesis is that historical restrictions in suitable habitat may generate further restriction of suitable habitat with the causal chain consisting of population bottlenecks, leading to reduced adaptive genetic variation, leading to reduced ability to fight diseases, thus affecting potential habitat choice

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5
Bulletin 100 April 2003
Piersma: “Coastal” versus “inland” shorebird species
5
“Coastal” versus “inland” shorebird species: interlinked fundamental
dichotomies between their life- and demographic histories?
THEUNIS PIERSMA1,2
1Department of Animal Ecology, Centre for Ecological and Evolutionary Studies, University of Groningen,
PO Box 14, 9750 AA Haren, The Netherlands, e-mail: theunis@nioz.nl; 2Department of Marine Ecology and
Evolution, Royal Netherlands Institute for Sea Research (NIOZ), PO Box 59, 1790 AB Den Burg, Texel,
The Netherlands
Piersma, T., 2003. “Coastal” versus “inland” shorebird species: interlinked fundamental dichotomies between
their life- and demographic histories? Wader Study Group Bull. 100: 5–9.
In this contribution I present an extended but testable hypothesis (or “evolutionary scenario”) to explain how
and why many life-history features of latitudinal migrant shorebirds, basically characterised by the correla-
tion between habitat choice in the winter and the breeding season, may be functionally and causally intertwined.
The most novel (and contentious) aspect of the hypothesis is that historical restrictions in suitable habitat may
generate further restriction of suitable habitat with the causal chain consisting of population bottlenecks, leading
to reduced adaptive genetic variation, leading to reduced ability to fight diseases, thus affecting potential habitat
choice.
INTRODUCTION
The life-histories of the 86 sandpiper species (Scolopacidae),
66 plovers (Charadriidae), 11 oystercatchers (Haemato-
podidae) and 7 stilts (Recurvirostridae) encompass a vast
spectrum of migration strategies, habitat selection, foraging
styles, degrees of plumage polymorphism and mating sys-
tems (see respectively Piersma et al. 1996, Piersma &
Wiersma 1996, Hockey 1996, Pierce 1996). Yet, these birds
also share many basic biological features: low reproductive
rates with a clutch of 3 or 4 eggs, open nests, precocial chicks
(Schekkerman et al. 2003), reliance on wetland ecosystems,
relatively high Basal Metabolic Rates (Kersten & Piersma
1994) and relatively long lives (Goede 1993). As shown
below, within the long-distance (latitudinal) migrant species
of the sandpiper and plover families, covariation in life-
history strategies can be detected, involving population size,
extent and predictability of selected habitats, and migration
distances. This cline in life history strategies is characterised
by the correlation between habitat choice in winter and in the
breeding season.
THE PATTERNS
Shorebird species breeding in the High Arctic usually spend
the winter in marine habitats, whereas species breeding south
of the tundra desert belt tend to winter in more freshwater
habitats (Piersma 1997). Note (1) that freshwater habitats
include lowland and upland grasslands used e.g. by tundra
plovers Pluvialis during the nonbreeding season and by cur-
lew species Numenius and Upland Sandpipers Bartramia
longicauda throughout the year and (2) that saline inland
habitats may well qualify (at least in terms of disease organ-
isms) as “marine” habitats.
Indeed, when the breeding and the wintering habitats of
the 24 different species of the sandpiper subfamily Calidrinae
are ranked as “decreasingly high arctic and alpine” and “de-
creasingly marine/saline”, the covariation is clearly shown
(Fig. 1). There are exceptions to the rule such as Buff-
breasted Sandpipers Tryngites subruficollis (number 23 in
Fig. 1) breeding in the High Arctic and wintering at inland
pasture sites in Patagonia, but the Spearman rank correlation
coefficient is 0.70, a value that is statistically significant from
zero (p<0.01). Red Knots Calidris canutus and Ruffs Philo-
machus pugnax occupy the extremes, the first being one of
the most highly arctic breeders wintering exclusively in
coastal marine environments, the second being the southern-
most breeding sandpiper species wintering exclusively in
inland and freshwater habitats. Of course, there is an element
of subjectivity in the ranking of the species’ habitat charac-
teristics. However, as the outlying groups are perfectly clear-
cut, the association demonstrated here seems robust.
In addition, shorebirds wintering in marine habitats tend
to have smaller population sizes than shorebirds wintering in
freshwater habitats (Piersma 1986). The low latitude/fresh-
water species tend to have shorter overall migration dis-
tances, which are covered by a greater number of shorter
flights than the high latitude/marine species (Piersma 1997).
Although the genetic variability in shorebirds appears to be
quite low overall (Baker & Strauch 1988), a comparison of
two sandpipers (Dunlin Calidris alpina and Red Knot) has
established that the northernmost breeding species (the Red
Knot) was hit by the severest population bottlenecks in the
late Pleistocene and Holocene (Baker & Marshall 1997).
Also, allozyme assays of genetic variation seem to show that
the Ruff, the southernmost breeding and most inland winter-
ing sandpiper species has much greater variation (Segre et al.
1970) than Dunlin and Red Knot (Baker 1992). Indeed,
within the genus Calidris, a measure of genetic variability,
mean heterozygosity as reported by Baker (1992), is posi-
tively correlated with the rank order of wintering habitat, i.e.
the relative use of freshwater habitats (Fig. 2; note that the
correlation with the rank order of breeding habitat is positive
but not significant).Wader Study Group Bulletin 6
Bulletin 100 April 2003
THE HYPOTHESIS
Based upon arguments developed earlier (Piersma 1997), I
suggest that the covariation between breeding latitude and
wintering habitat may reflect co-evolved life history com-
plexes along correlated latitudinal (with respect to breeding
area) and marine-freshwater habitat (nonbreeding areas)
axes. For heuristic purposes, one can take the extremes of the
latitude/habitat axes to develop a hypothesis about the evo-
lutionary linkages between demographic bottlenecks, disease
and nutritional factors and ecological characteristics (Fig. 3).
Although freshwater wetland habitats used by shorebirds are
usually ephemeral and unpredictable, low-latitude breeding
species using these habitats have large parts of continents to
live in. This would explain the relatively large population
sizes and the possible paucity of historical population bottle-
necks (the latter remains to be established).
In contrast, extreme habitat specialists that breed on high
arctic tundra and winter in (coastal) marine habitats are lim-
ited to suitable parts of the continental fringes where inter-
tidal soft sediments or rich rocky shorelines occur. The avail-
able area of habitat is one- rather than two-dimensional and
thus much smaller than that of inland winterers. This is true
not only in winter but also during migration – long flights are
necessary to bridge the distances between suitable staging
areas. During times of rapid climate change and shrinking
habitats, their already small populations would become even
further reduced. If severe population bottlenecking contin-
ued, serial loss of adaptive genetic variation in the genes
coding for the immune system (i.e. genes coding for antigen
recognition sites or natural antibodies) could occur (O’Brien
& Evermann 1988). The recently population-bottlenecked
Red Knot is a case in point (Baker et al. 1994, see Avise 2000)
and could be called the avian equivalent of the Cheetah
Acinonyx jubatus. Cheetahs exhibit very low levels of
genetic variation, probably because of a severe recent popu-
lation bottleneck also (Caro 1994). This low genetic varia-
tion appears correlated with increased susceptibility to infec-
Fig. 1.  Correlation between the extent to which shorebird species belonging to the subfamily Calidrinae (Scolopacidae) breed in decreasingly
arctic/alpine, open and climatically extreme habitats (rank order breeding habitat) and the extent to which they winter increasingly in fresh-
water rather than marine habitats (rank order wintering habitat). The linear regression line is shown to lead the eye. Rank orders com-
piled from data in Piersma et al. (1996) using the midpoint of the breeding ranges to assess the rank number of breeding habitat. 1: Aphriza
virgata; 2: Calidris tenuirostris; 3: Calidris canutus; 4: Calidris alba; 5: Calidris pusilla; 6: Calidris mauri; 7: Calidris ruficollis; 8: Calidris
minuta; 9: Calidris temminckii; 10: Calidris subminuta; 11: Calidris minutilla; 12: Calidris fuscicollis; 13: Calidris bairdii; 14: Calidris melanotos;
15: Calidris acuminata; 16: Calidris ferruginea; 17: Calidris maritima; 18: Calidris ptilocnemis; 19: Calidris alpina; 20: Eurynorhynchus
pygmeus; 21: Limicola falcinellus; 22: Micropalama himantopus; 23: Tryngites subruficollis; 24: Philomachus pugnax.7
Bulletin 100 April 2003
Piersma: “Coastal” versus “inland” shorebird species
tious diseases (O’Brien et al. 1985), perhaps caused by re-
duced variability in the Major Histocompatability Complex
(MHC, the part of the genome that codes for adaptive immu-
nity; see e.g. Zelano & Edwards 2002). Additionally, or alter-
natively, in high latitude/marine species the expression of
immunocompetence may be further compromised due to
long flights necessitating extreme physical performance and
nutritional imbalances (Piersma 1987).
If an increased susceptibility to disease restricted the
range of suitable habitats (e.g. birds having to avoid areas
with ample food but many [vectors for] debilitating diseases,
such as mosquitoes carrying avian malaria), we have a sys-
tem with a strong positive historical feedback link (Fig. 3).
This is rather more exciting than a system where historical
ecological constraints have simply led to a loss of genetic
variation for disease resistance; that is, lowered disease re-
sistance being just a consequence (and not also a cause) of
population bottlenecks due to temporary restrictions in habi-
tat availability.
Thus, habitat selection, population size, migration strat-
egies and disease resistance may all be linked to the same
historical web of causality. In fact, there are several addi-
tional biological contrasts that may be relevant: the more
pronounced seasonal plumage dimorphy in the high latitude
breeding species (Jukema & Piersma 2000), their greater
apparent organ flexibility (Piersma 1998) and the suggestion
that freshwater species seem to first migrate northwards from
the circa-tropical wintering areas at earlier ages than the
coastal species (D.I. Rogers pers. comm.). Also, freshwater
species of shorebirds appear to have a lower “lifespan energy
potential” (spend less energy per maximum lifetime) than
marine species (Goede 1993).
DISCUSSION
What I have outlined here is a hypothesis that connects sev-
eral life-history observations on latitudinal migrant shore-
birds with some mechanistic biological processes. Some
parts of the overall hypothesis (or evolutionary scenario) are
well established, but bigger parts need filling in. Whatever
its truth, the hypothesis should be challenging and stimulat-
ing, and encourage a wide range of research activities to be
started up and research outcomes to be connected. Although
it might not be immediately obvious that the system sug-
gested, or the problems posed, will be amenable to insight-
ful investigation, I strongly believe that careful use of nested
hierarchies of tests of competing hypotheses would help us
to make rapid progress with this research programme. For
example, at the level of interspecific comparisons, impaired
immunocompetence in arctic/marine species could result
from either serial losses of genetic variation or from reduced
expression under nutritional stress or increased exercise. The
competing hypotheses can be tested in a series of compari-
sons of species pairs, where immunocompetence assays
would be carried out in exercised vs. unexercised, or well fed
vs. nutritionally constrained individuals. Such tests could be
carried out for species pairs of other groups of animals that
have similar ecological dichotomies. There is a research pro-
gramme with comparable lines of thinking that is currently
underway, comparing the life histories of temperate and
tropical passerines in the Americas (R.E. Ricklefs pers.
comm.).
Relevant pairwise species comparisons could be made for
(1) current population trends and demography, (2) habitat
selection, (3) migration strategies, (4) past demographic
Fig. 2.  Relationship between the mean heterozygosity of Calidris species (a measure of genetic variability; from Baker 1992: Table 1)
and the rank number of the wintering habitat (where the lowest numbers refer to the most marine habitat choice) as the y-axis in Fig. 1
(Spearman rank correlation coefficient is 0.58, n = 13, p < 0.05). The linear regression line is shown to lead the eye.Wader Study Group Bulletin 8
Bulletin 100 April 2003
Fig. 3.  Schematic overview of the contrasts between latitudinal migrant shorebird species that breed at high latitudes and spend the win-
ter in marine (saline) habitats and those that breed at lower latitudes and spend the winter in freshwater (including grassland) habitats
and the possible consequences and positive feedbacks induced by population bottlenecks.9
Bulletin 100 April 2003
Piersma: “Coastal” versus “inland” shorebird species
bottlenecks, (5) MHC variation and (6) various aspects of
immunocompetence. Based on the latest phylogeny for the
170 species of shorebirds (T. Paton & A.J. Baker in prep.),
the following species pairs would be relevant and useful for
studies in Western Europe (with the first species denoting the
arctic/marine member of the pair): sandpipers (Red Knot vs.
Ruff), godwits (Bar-tailed Godwit Limosa lapponica vs.
Black-tailed Godwit L. limosa), tundra plovers (Grey Plover
Pluvialis squatarola vs. Eurasian Golden Plover P. apri-
caria) and ringed plovers (Ringed Plover Charadrius hiati-
cula vs. Little Ringed Plover Ch. dubius). A similar range of
questions can be asked about intra-specific systems. For
example, we can use species with a very wide latitudinal
breeding range (Dunlin, Ringed Plover and Ruddy Turnstone
Arenaria interpres), where the northernmost populations
usually winter furthest south (leap-frog migration), for paired
comparisons between northern and southern populations (or
subspecies). Red Knots, that offer six different subspecies
with slightly different population histories (D.M. Buehler &
A.J. Baker pers. comm.) and a large range in migration dis-
tances (Piersma & Davidson 1992), may enable an intraspe-
cific test of the roles of exercise and energy expenditure on
disease susceptibility in a bottlenecked species.
ACKNOWLEDGEMENTS
Allan J. Baker, Robert E. Ricklefs, Christiaan Both, Kirk C.
Klasing and Debbie M. Buehler have been supportive and
critical discussants during the times these ideas were brew-
ing. I thank Luisa Mendes for actually and successfully open-
ing, as a PhD student, the can-of-worms of shorebird com-
parative parasitology and immunology, Danny I. Rogers for
sharing ideas, Dick Visser for figure design and preparation,
and Brett Sandercock and John D. Goss-Custard for helpful
reviews.
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can Naturalist 160: S225–S237.

An Mhc component to kin recognition and mate choice in birds: predictions, progress, and prospects.

Breeding waders in Europe: a review of population size estimates and a bibliography of information sources.

Cheetahs of the Serengeti Plains. Group living in an asocial species. Chicago:

Contour feather moult of Ruffs Philomachus pugnax during northward migration, with notes on homology of nuptial plumages in scolopacid waders.

Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure?

Family Charadriidae (plovers). In

Family Haematopodidae (oystercatchers) In

Family Recurvirostridae (stilts and avocets)

Family Scolopacidae (sandpipers, snipes and phalaropes). In

Genetic basis for species vulnerability in the Cheetah.

Genetic variation and differentiation in shorebirds.

High levels of energy expenditure in shorebirds; metabolic adaptations to an energetically expensive way of life.

Interactive influence of infectious disease and genetic diversity in natural populations.

Isozyme polymorphism in the Ruff (Aves: Philomachus pugnax): a species with polymorphic plumage.

Longevity in homeotherms, the high lifespan and lifespan energy potential in Charadriiformes.

Mechanisms promoting higher growth rates in arctic than in temperate shorebirds.

Mitochondrial control region sequences as tools for understanding evolution.

Molecular genetics of Calidris, with special reference to Knots.

Phenotypic flexibility during migration: optimization of organ size contingent on the risks and rewards of fueling and flight?

Phylogeography. The history and formation of species.

The migrations and annual cycles of five subspecies of Knots in perspective.

Unraveling the intraspecific phylogeography of Knots Calidris canutus: a progress report on the search for genetic markers.

“Coastal” versus “inland” shorebird species: interlinked fundamental dichotomies between their life- and demographic histories?

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“Coastal” versus “inland” shorebird species: interlinked fundamental dichotomies between their life- and demographic histories?

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