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Osmoregulatory capacity and the ability to use marine food sources in two
coastal songbirds (Cinclodes: Furnariidae) along a latitudinal gradient
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E C O PH Y SI OL O G Y
Received: 30 August 2005 / Accepted: 23 January 2006 / Published online: 23 February 2006
Springer-Verlag 2006
Abstract Cinclodes nigrofumosus and C. oustaleti are two decreased from north to south, and kidney size increased
closely related songbirds that inhabit the northern significantly with latitude. Cinclodes nigrofumosus had
Chilean coast during the austral fall and winter.This larger kidneys with larger proportions of medullary tis-
stretch spans a dramatic north to south latitudinal gra- sue than C. oustaleti. C. nigrofumosus and C. oustaleti
dient in rainfall and temperature. Whereas C. nigro- are terrestrial organisms subsidized by a rich marine
fumosus lives exclusively on coastal environments, C. environment where it is adjacent to an unproductive
oustaleti shifts seasonally from coastal environments to terrestrial. Variation in the reliance on marine food
inland freshwater ones. We used the d13C of these two sources seems to be accompanied by adjustments in the
species’ tissues to investigate whether the reliance on osmoregulatory mechanisms used by these birds to cope
marine versus terrestrial sources varied from the hyper- with salt and dehydration.
arid north to the wet south. We also investigated lati-
tudinal variation in the renal traits that mediate how Keywords Cinclodes Æ Latitudinal gradient Æ
these birds cope with dehydration and a salty marine Marine-terrestrial nutrient transfer Æ Osmoregulation Æ
diet. Both species increased the incorporation of terres- Stable isotopes
trial carbon, as measured by d13C, as terrestrial pro-
ductivity increased southwards. However, C.
nigrofumosus had consistently more positive (i.e. more Introduction
marine) and less variable d13C values than C. oustaleti.
The osmoregulatory traits of both species varied with Marine environments can be very productive and often
latitude as well. Urine osmolality decreased from subsidize consumers in more unproductive contiguous
extremely high values in the north to moderate values terrestrial ecosystems (Polis and Hurd 1996). However,
in the south, while C. nigrofumosus produced more the terrestrial animals that take advantage of marine
concentrated urine than C. oustaleti. In both species, foods must get rid of high salt loads (Nystrom and Pe-
the proportion of kidney devoted to medullary tissue hrsson 1988; Mahoney and Jehl 1985). Diets of marine
origin can impose an exceptional osmoregulatory chal-
lenge to songbirds (Order Passeriformes), which lack
functional salt glands (Shoemaker 1972) and have a
Communicated by Jim Ehleringer limited ability to concentrate urine (Goldstein and
Skadhauge 2000). Among passerines, the genus Cincl-
P. Sabat (&) Æ K. Maldonado
Departamento de Ciencias Ecológı́cas, Facultad de Ciencias,
odes (Furnariidae) is well suited to investigate the
Universidad de Chile, Casilla 653, Santiago, Chile interplay of osmoregulation, water availability, and diet
E-mail: psabat@uchile.cl in terrestrial organisms that feed on marine diets. This
genus is unique because it includes coastal species that
J. M. Fariña feed almost exclusively on marine invertebrates (Sabat
Center for Advanced Studies in Ecology & Biodiversity
and Departamento de Ecologı́a, Facultad de Ciencias Biológicas, et al. 2003), species that inhabit inland freshwater envi-
Pontificia Universidad Católica de Chile, Santiago, Chile ronments and feed on insects, and species that shift
seasonally between coastal and inland environments and
C. M. del Rio feed on both insects and marine invertebrates (Sabat and
Department of Zoology and Physiology, University of Wyoming,
Laramie, WY 82071, USA Martinez de Rı́o 2002; Sabat and Martı́nez del Rio
E-mail: cmdelrio@uwyo.edu 2005).
251
P. Sabat (unpublished results) contends that Cincl- primarily marine diet (Sabat and Martı́nez del Rio
odes represents an adaptive radiation in which ecological 2002). C. oustaleti shifts habitats seasonally. During the
diversification has been mediated by evolutionary winter, it shares C. nigrofumosus’ habitat, but in contrast
changes in osmoregulatory function. They compared the with this habitat specialist, C. oustaleti also occupies
traits of five Cinclodes species and found that the renal freshwater and brackish estuaries (P. Sabat and C.
traits associated with the capacity to concentrate urine Martı́nez del Rio, unpublished observations). During
were tightly correlated with reliance on a marine diet as the austral spring and summer, C. oustaleti moves inland
estimated by the carbon isotope composition of the to freshwater streams and bogs. C. nigrofumosus and C.
bird’s tissues (P. Sabat, unpublished results). The oustaleti can be characterized as a habitat specialist and
objective of this contribution is to describe the variation a generalist, respectively.
in reliance on marine sources as estimated by stable Our study was guided by three questions: (1) Does
isotopes in two Cinclodes species, C. nigrofumosus and reliance on marine sources vary with the availability of
C. oustaleti, along a dramatic latitudinal gradient in freshwater along the gradient; (2) does the latitudinal
water availability and temperature (Fig. 1). We also pattern of variation of C. nigrofumosus, a habitat spe-
portray changes along this gradient in two renal features cialist differ from that of C. oustaleti, a habitat gener-
that are associated with the capacity to cope with salty alist; and (3) is water availability and/or reliance on a
diets and dehydration: kidney size and the proportion of marine diet associated with the traits that correlate with
renal tissue allocated to medulla (Sabat and Martı́nez the ability to cope with salty diets, such as kidney size
del Rio 2002; P. Sabat, unpublished results). We ask and the proportion of kidney devoted to medullary tis-
whether the patterns revealed by these interspecific sue (P. Sabat, unpublished results)? Question 1 cannot
comparisons also hold within a single species. be answered unambiguously a priori. On the one hand,
We chose C. nigrofumosus and C. oustaleti because the availability of freshwater can facilitate a marine diet
they are syntopic during the austral winter and, because by providing water to flush out dietary salts and by
in addition to inhabiting the same habitat seasonally, ‘‘diluting’’ the salt loads in osmoconforming inverte-
they seem to differ in their specialization to a marine diet brates in areas close to estuaries (Sabat and Martinez del
(P. Sabat, unpublished results). C. nigrofumous inhabits Rio 2005, and references therein). On the other, rainfall
only wave-swept rocky shorelines, where it feeds on is accompanied by increased productivity in terrestrial
marine invertebrates including molluscs and crustaceans habitats (Lieth 1978; Polis and Hurd 1996) and hence
(Sabat et al. 2003). To our knowledge, C. nigrofumosus is with increased availability of terrestrial prey. We
the only documented passerine species to have a hypothesized that, during the winter, when the two
species are syntopic, C. nigrofumosus which lives year Chañaral as very dry (DMAI equals 0.92 and 0.06,
round in inter-tidal environments, would be more respectively). It characterizes La Serena and los Vilos as
dependent on marine sources than C. oustaleti, which dry (DMAI = 5.13 and 8.33, respectively), and El
migrates seasonally between freshwater and marine Quisco and Lebu as humid (DMAI = 33.43 and 56.62,
environments. We also hypothesized that C. oustaleti respectively). The vegetation along the gradient ranges
would have higher variance in the use of marine and from very scanty in the hyperarid north, to Mediterra-
terrestrial sources than C. nigrofumosus. In a previous nean scrub with increased productivity from La Serena
comparative study, Sabat and Martı́nez del Rio (2002) to Lebu. Immediately after capture, a sample of ureteral
found that within the genus Cinclodes, the ability to urine was obtained by inserting a small closed-ended
produce concentrated urine, and hence to cope with cannula into the birds’ cloaca (Goldstein and Braun
aridity and with diets with high salt loads, was corre- 1989; Sabat and Martinez del Rı́o 2002). Urine drained
lated with both the relative size of the kidney, with the into the cannula via a window placed dorsally over the
fraction of the kidney allocated to medullary tissue, and ureteral orifices (Goldstein and Braun 1989). Urine
with the relative number of medullary cones (see also samples were centrifuged and the osmolality of the
Goldstein and Skadhauge 2000). The positive associa- supernatant was measured (Wescor 5130B). Kidneys
tion between relative kidney size and percentage of were weighed (±0.001 g) and preserved in paraformal-
medullary tissue with concentrating ability is consistent dehyde-glutaraldehyde. We estimated the area of me-
with previous observations on both passerines (reviewed dulla by point counting using the Cavalieri Principle on
by Casotti and Braun 2000; Sabat 2000) and non- the right kidney, which was processed for routine light
passerines (Hughes 1970). Consequently, we also pre- microscopy (Gundersen et al. 1988; Wauri 1989). The
dicted that kidney size and the proportion of kidney percentage of renal medulla was determined as the area
devoted to medullary tissue would decrease from north of medullary tissue divided by the total area of the
to south with increased precipitation (P. Sabat, unpub- kidney section. A sample of pectoralis muscle was de-
lished results). fatted by petroleum ether extraction, freeze-dried,
Our study relied on carbon stable isotope ratios as ground into a fine powder, and loaded (0.15 mg) into
indicators of diet (marine vs terrestrial) and as indirect pre-cleaned tin capsules for isotopic analysis. We
indices of the salt loads experienced by birds (Sabat and determined the diet of a sub-sample of collected indi-
Martı́nez del Rio 2002). Using the carbon isotope ratio viduals. Food was extruded from the crop, gizzard and
of a consumer’s tissues to assess the relative contribution proventriculus and stored frozen in liquid nitrogen. Gut
of marine and terrestrial sources relies on two observa- contents were thawed and prey items were separated,
tions: (1) tissues reflect the isotopic composition of an weighed (±0.0005 g) and identified to the lowest taxo-
animal’s diet (Hobson and Clark 1992), and (2) marine nomic level possible. In addition to documenting diet
food sources are significantly enriched in 13C relative to composition qualitatively (Table 1), we also estimated
sources from contiguous terrestrial habitats (i.e., d13C is the percent by weight of items of marine or terrestrial
more positive; Blundell et al. 2002,and references origin. Carbon isotope ratios were measured on a con-
therein). Our study depends on the large difference in tinuous flow isotope ratio mass spectrometer (VG Iso-
isotopic composition between marine seagrasses and tech, Optima) with samples combusted in a Carlo Erba
macroalgae at the base of intertidal food webs NA 1500 elemental analyzer at the Columbia University
(d13cranges from 10 to 15&) and the C3 vegetation Biosphere 2 stable isotope facility. The precision of these
of the coast of Chile (24 to 27&). analyses was ±0.3 (&) (SD). Laboratory standards,
vacuum oil (d13C=27.5 &) and sucrose
13
(d C=10.5&, National Institute of Standards and
Materials and methods Technology 8542) were included with each run. Stable
isotope ratios were expressed using standard delta
Animals were collected between 2000 and 2003 in the notation (d) in parts per thousand (&) as:
austral winter and fall (between June and September) at
five sites along the coast of Chile (Fig. 1): Taltal 13 Rsample
d C¼ 1 1; 000
(2525¢S, 7034¢W), Chañaral(2620¢S, 7037¢W), La Rstandard
Serena (2954¢S, 7115¢W), Los Vilos (3153¢S,
where Rsample and Rstandard are the molar ratios of
7130¢W), El Quisco (3334¢S, 7137¢W), and Lebu 13
C/12C of the sample and reference, respectively. Sam-
(3737¢S, 7340¢W). We collected C. nigrofumosus at all
ples were referenced against the international standard,
sites, but we were unable to collect C. oustaleti at Taltal.
the Vienna Pee DeeBelemnite (VPDB).
Our study sites vary not only in rainfall and tempera-
ture, but also in the length of the season during which
each site can be considered arid. For example, Taltal and
Chañaral are dry year round, whereas Lebu’s dry season Statistical analyses
extends only from December to March (di Castri and
Hayek 1976). De-Martonne’s aridity index (DMAI; di We were interested in finding out the potential effect of a
Castri and Hayek 1976) characterizes Tal Tal and latitudinal gradient in rainfall and temperature on the
253
Table 1 The organisms found in the gastrointestinal contents of reveal whether C. nigrofumosus and C. oustaleti dif-
Cinclodes nigrofumosus and C. oustaleti at all study sites included fer—or not—along a latitudinal gradient. They do not
both marine invertebrates and insects
permit inferring whether habitat generalists differ from
C. oustaleti C. nigrofumosus habitat specialists in their response to a latitudinal gra-
(n=36) (n=20) dient in aridity.
Prey FO % FO FO % FO
Algae Results
Ulva sp. 6 16.7 11.0 55.0
Chondrus caniculatus 1 2.8 1.0 5.0 Table 1 lists the identity and frequencies of prey items
Crustaceans found in the gastrointestinal of both species at all sites.
Allopetrolisthes spinifrons – 7.0 35.0
A. angulosus 1 2.8 3.0 15.0 We were able to analyze the percentage of marine and
A. punctatus – 1.0 5.0 terrestrial items in the gastrointestinal contents of 67 C.
Grapsus grapsus – 2.0 10.0 nigrofumosus individuals collected at all sites, except
Leptograpsus variegatus - 5.0 25.0 Chañaral. Unfortunately, the sample of C. oustaleti gut
Cyclograpsus cinereus 1 2.8 2.0 10.0
Rinchocinettes typus – 1.0 5.0 contents from which we were able to estimate the
Paraxanthus barbiger 1 2.8 – quantitative contribution of each prey type to the total
Acanthocyclus gay 2 5.6 – mass of food in the gastrointestinal tract was restricted
Barnacles 0.0 1.0 5.0 to 20 individuals from a single site (El Quisco). Because
Mollusks
Nodilittorina araucana 4 11.1 10.0 50.0
we did not have adequate representation of both species
N. peruviana - 2.0 10.0 at all sites, we used inferential statistics to compare be-
Prisogaster niger 1 2.8 1.0 5.0 tween the gut contents of C. nigrofumosus and C.
P. gigas - 1.0 5.0 oustaleti only at El Quisco. At El Quisco, the gut con-
Scurria variabilis - 2.0 10.0 tents of C. nigrofumosus (n=19) had higher percentages
S. ceciliana 4 11.1 1.0 5.0
S. zebrina - 1.0 5.0 of crustaceans (mean%±SD=57.2±34.2%, t=3.6,
Semimytilus algosus - 1.0 5.0 P<0.002) and of total marine foods (62.8±35.9%,
Insects t=3.8, P<0.001) than those of C. oustaleti
Diptera (adults) 15 41.7 4.0 20.0 (12.1±29.0% and 18.7±31.8% for crustaceans and
Diptera (larvae) 8 22.2 9.0 45.0
Coleoptera 3 8.3 3.0 15.0 marine items, respectively). In contrast, the guts of C.
Isopoda – 6.0 30.0 oustaleti contained a higher percentage of insects
(72.5±34.6) than those of C. nigrofumosus (19.3±22.4).
FO is the absolute frequency of occurrence in gut contents and % The percentage of molluscs in the gut contents of C.
FO is the percent of occurrence. Although the marine algae, Ulva
sp. and Chondrus caniculatus, appear frequently in gut contents, oustaleti (10.6±23.4) did not differ significantly from
their contribution by mass was small and we suspect that they were that in the gut of C. nigrofumosus (23.3±27.3, t=1.3,
ingested accidentally (1.6 and 0.2% of total mass in C. oustaleti and P=0.21).
C. nigrofumosus, respectively) Variation in reliance on marine against terrestrial
sources along the latitudinal gradient was apparent in
characteristics of C. nigrofumosus and C. oustaleti. both C. nigrofumosus and C. oustaleti. The d13C of
However, both of these variables covary tightly along pectoralis muscle decreased significantly with latitude in
our gradient, and both covary tightly with De Mar- both species (F1,84(latitude)=10.24, P=0.002; Fig. 2).
tonne’s aridity index (di Castri and Hayek 1976; Fig. 1). The tissues of C. nigrofumosus were enriched in 13C over
Thus, we used latitude as a surrogate variable for arid- those of C. oustaleti by approximately 2.5& throughout
ity. Latitude has the added virtue that it is measured the gradient (F1,84(species)=94.36, P<0.001; Fig. 2).
without error, whereas rainfall, temperature, and DMAI The variance in the residuals of the d13C against latitude
are measured as averages with associated variances. regression line estimates variance in the use of marine
Using latitude allowed us to use least squares regression and terrestrial food sources. Cinclodes oustaleti was
and its associated linear models (Sokal and Rohlf 1995). more variable in its incorporation of marine carbon than
Analyses conducted using average annual rainfall and C. nigrofumosus (F56,30=36.63, P<0.001; Fig. 2).
DMAI as independent variables are consistent with the The changes in reliance on marine against terrestrial
results described here. Our study compares the responses sources along the gradient appeared to also be accom-
of two closely related congeners to a gradient in aridity. panied by changes in the ingestion of salts and/or by
In most comparisons we used a linear model to assess changes in evaporative water losses and hence in the
the effect of latitude on a trait and to compare among need to produce more concentrated urine. The osmo-
species. Whenever the interaction term between species lality of ureteral urine decreased significantly with lati-
and latitude was non-significant, we dropped it from the tude in both species (F1,84(latitude)=47.24, P<0.001;
model (Zar 1996). Two species comparisons have been Fig. 2). However, C. nigrofumosus produced urine that
belittled as uninformative (Garland and Adolph 1994). was 100 mOsm/kg more concentrated than that pro-
Although we recognize their limitations, we find two duced by C. oustaleti (F1,84(species)=8.15, P=0.006;
species comparisons informative. Our comparisons Fig. 2).
254
favor of each of these explanations is scanty we offer interaction (Garland and Adolph 1991). What is the
them more as testable hypothesis than as established contribution of each of these effects to the latitudinal
facts. C. nigrofumosus and C. oustaleti offer a good variation observed in C. nigrofumosus and C. oustaleti?
opportunity to investigate the role that agonistic Sabat et al. (2004a) provided adult C. nigrofumosus and
behavior and physiological differences in the ability to C. oustaleti individuals with either tap water or a salt
use a resource play in determining niche breadth in two solution (NaCl, 800 mOsm/kg) for 2 weeks. The C.
syntopic congeners (Taniguchi and Nakano 2000). oustaleti individuals exposed to salt water had larger
renal medullae and were able to produce more concen-
trated urine than those exposed to tap water (Sabat et al.
Are aridity and/or reliance on a marine diet associated 2004a). However, the effect of exposure to fresh or salt
with relative kidney size and the proportion of kidney water on medullary size was relatively small (22%) and
devoted to medullary tissue? smaller than the differences found along the extremes of
the latitudinal gradient (120%). The renal character-
Both relative kidney size and the proportion of kidney istics of C. nigrofumosus individuals exposed to fresh or
devoted to medullary tissue varied from north to south. salt water did not differ (Sabat et al. 2004a). These
As expected, relative medullary size decreased from the experiments suggest that phenotypic flexibility (sensu
more arid north where birds relied more on salty marine Piersma and Drent 2003) in adult birds is unlikely to
diets to the more mesic south where birds included more explain all the variation in renal traits observed along
terrestrial prey in their diets. The significant latitudinal the latitudinal gradient. However, we cannot yet dis-
variation in urine osmolality along the gradient supports count the possibility that exposure to different environ-
the notion that the dry north represents an environment ments during early development (or developmental
where birds are challenged by both the absence of fresh plasticity, sensu Piersma and Drent 2003) contributes to
water and the ingestion of salty prey (Cassoti and latitudinal variation in renal traits. At the moment, we
Richardson 1992). Indeed, at the two dry sites, Taltal and cannot partition the effect of phenotypic plasticity and
Chañaral, birds produced urine with osmolalities that are population differentiation on the magnitude of latitudi-
at the high end of, or even exceed, those reported for all nal gradient in kidney morphology, and hence in the
bird species (Goldstein and Skadhauge 2000). capacity to cope with dehydration and salty diets, found
Against our expectations, birds had relatively larger in C. nigrofumosus and C. oustaleti.
kidneys in the mesic south than in the arid north. This Our results imply that variation in reliance on marine
result is concordant with the observation that animals food, both along an aridity gradient and between spe-
that face antidiuresis chronically in dry environments cies, is accompanied by adjustments in the osmoregula-
tend to have smaller kidneys than those that live in tory mechanisms that animals use to cope with salt and
wetter environments (reviewed by McNab 2002), but dehydration. Most studies on the subsidies by produc-
appears to contradict the interspecific patterns found by tive marine environments to unproductive terrestrial
P. Sabat (unpublished results). Sabat also found a po- ones have emphasized nutrient transfer (reviewed by
sitive interspecific correlation between the d13C of tissues Polis et al. 2004). Our study reveals that sometimes this
and relative kidney size. The discrepancy may reveal a transfer of energy and nutrients also involves the
difference between interspecific and intraspecific levels of movement of other less desirable materials, such as
analysis. At the interspecific level, the positive associa- excessive salt. Our results highlight that marine-to-ter-
tion between d13C and kidney size probably reflect the restrial nutrient transfer studies sometimes need to
increased kidney size required by the amount of med- consider the physiological mechanisms that mediate how
ullary tissue needed to process salty marine diets. Within terrestrial organisms cope with marine diets.
C. nigrofumosus and C. oustaleti, the increase in kidney
size from north to south probably reflects higher rates of Acknowledgements We were financed by Fondo Nacional de De-
water loads and hence higher water processing rates in sarrollo Cientı́fico y Tecnológico (Chile proyecto no. 1010647) to
PSK and FONDECYT (no. 1040783) to JMF, and by a National
the more mesic south (McNab 2002). The disparity in Science Foundation Grant (IBN 0421738) to CMR. Birds were
our interspecific and intraspecific analyses reflects our captured with permits from SAG, Chile (permit no. 674/2001-
inadequate understanding of how the needs to dispose of 2005). All protocols were approved by the Institutional Animal
and conserve water, and to get rid of salt, influence and Care Committees of the Universidad de Chile and the University of
Wyoming. We thank Sofia Sabat (aged 4) for spotting birds for us
are influenced by kidney morphology and function in and for deflating C.M.R.’s ego.
birds (Goldstein and Skadhauge 2000).
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