Stable Isotopes and the Determination of Avian Migratory Connectivity and Seasonal Interactions

Until the mid-1990s, our ability to make migratory connections and evaluate seasonal interactions was limited by conventional markrecapture techniques applied to focal populations. Although this approach can be powerful, it is typically most effective when applied to large data sets, usually available only for game species (Hobson 2003). The recent development of stable-isotope analysis (SIA) techniques has changed that situation, because the SIA approach does not rely on mark-recapture but only on the single capture of individuals to infer breeding (or occasionally wintering) origin. This approach has been the subject of several recent reviews (Hobson 1999, 2003, 2005a; Rubenstein and Hobson 2004), and the interested reader is referred to these as well as to Kelly (2000) and Martínez del Rio and Wolf (1995) for more background on isotopic applications to migratory connectivity in particular, and more broadly to avian nutritional ecology. In addition to defining origins of individuals, the isotopic quantification of endogenous and exogenous contributions to eggs provided the first direct measurements of potential seasonal interactions involving females that travel to breed (Gauthier et al. 2003, Hobson 2005b). This is a very rapidly evolving field (Fig. 1) and has not been without its growing pains. Just how powerful is this approach and to what degree can it answer key questions associated with migratory connectivity and seasonal interactions? Number of published studies focusing on the application of stable-isotope analyses to track movements in birds by year. Estimates were based on a review of the literature, including searches using the Web of Science database. Review papers are also included in the annual counts (from Mazerolle 2005; see also Martínez del Rio and Wolf 2004). The principle behind the application of SIA of avian tissues to infer migratory connectivity is simply that isotopic patterns in nature can be variable; when a bird moves between one known “isotopic landscape” or “isoscape” (G. J. Bowen pers. comm.) and another, its tissues will retain isotopic information from the previous location for a period depending on the elemental turnover in that tissue. For feathers, isotopic information is usually “locked in,” because feather keratin is metabolically inert following formation; so this material is particularly useful when molt chronology and general location (breeding vs. wintering grounds vs. en route) are unambiguous. Fortunately, birds are amenable to captive study where their diets can be switched isotopically, thus mimicking a locational shift between isoscapes. To date, such studies have been conducted on various captive birds including Japanese Quail (Coturnix japonica), Great Skua (Stercorarius skua), Dunlin (Calidris alpina), Canvasback (Aythya valisineria), Garden Warbler (Sylvia borin), and Yellow-rumped Warbler (Dendroica coronata coronata) (reviewed by Evans Ogden et al. [2004]). Although this is a diverse taxonomic group, the combined results suggest that elemental turnover rate is associated with metabolic rate and that this follows the expected allometric relationship to body size (K. A. Hobson unpubl. data). The problem, of course, is that such turnover rates usually apply to birds fed ad libitum and not forced to exercise; these experimental conditions in no way approximate migration. This was potentially a problem with the interpretation of the study by Marra et al. (1998) that showed a weak but significant relationship between arrival time and muscle δ13C values of American Redstarts (Setophaga ruticilla) arriving at Hubbard Brook, New Hampshire. Marra et al. (1998) reasoned that the pattern of increasing δ13C values with arrival time was consistent with later arrival of birds wintering in poorer, more xeric habitats and provided the first direct evidence of seasonal interactions in a migratory passerine. Recently, K. A. Hobson and E. Yohannes (unpubl. data) conducted a diet-switch experiment on Rose-coloured Starlings (Sturnus roseus) trained to use a wind tunnel. Interestingly, that study showed no difference in blood isotopic turnover rate between exercised (3–4 h per day flying) and nonexercised groups, which suggests that such activity levels do not result in increased blood-cell replacement. If migration does not involve significant protein catabolism and is essentially fueled by fats stored after stopover, turnover rates for blood or muscle measured in captive, nonexercised, birds may well be appropriate for modeling the temporal window represented by tissue isotopic measurements (Hobson 2005a). A potentially more serious problem facing investigators using isotopic measurements of avian tissues to model seasonal interactions is the establishment of appropriate isotopic discrimination factors linking dietary isotope values with avian tissue values. Again, these values have been defined empirically using captive birds (reviewed by Evans Ogden et al. 2004), but recently it has been shown that diet quality, expressed in terms of the total carbon-tonitrogen ratio (C:N), can affect these discrimination factors (Pearson et al. 2003; but see Hobson and Bairlein 2004, Robbins et al. 2005). This is less of an issue for birds with consistently high- protein (i.e. high N) diets than for those that switch between insect (low C:N) and plant or fruit (high C:N) diets. If isotopic discrimination values can change depending on nutritional status, it may be difficult to tease out diet change from a physical change in location associated with a bird's movement to a new isoscape. Until further experimental research is conducted, establishing migratory connectivity for birds that switch diets seasonally may be problematic, at least for isotopes that are typically used for biome or habitat associations (e.g. δ15N and δ13C) and for tissues that are metabolically active. Describing isoscapes relevant to making migratory connections depends on the spatial scale of interest and the mechanisms driving isotopic heterogeneity in food webs. In terrestrial systems, variation in food-web δ13C values are driven largely by differences among plant photosynthetic pathways (C3, C4, CAM), but several other processes can contribute to isotopic variation among plants. Plants show very similar C3-based δ13C values in temperate areas of the continent. Hotter, more xeric areas can show more enriched values; this can result from plant water-use efficiency mechanisms that enrich δ13C values of C3 plants toward more C4 values. These general patterns are well known and it is reasonably straightforward to trace birds that may have moved between C3- and C4- or CAM-dominated regions (e.g. Wolf and Martínez del Rio 2000). Similarly, we also know that food-web δ15N values are influenced by climate, degree of soil exposure, and more and more by anthropogenic input of nitrogen to the biosphere (Nadelhoffer and Fry 1994). For both δ15N and δ13C measurements, agriculture—involving the use of nitrogen-based fertilizers and the planting of both C3 and C4 crops— contributes to isotopic complexity at landscape scales and beyond. Indeed, a strong case can be made that δ15N and δ13C isoscapes in North America, and indeed throughout the world, are simply too complex to be used reliably to track migratory birds, and most researchers tend to shy away from interpreting these sorts of data. Koch et al. (1995) pointed out that the usefulness of the much-celebrated forensic technique of using SIAs of African elephant (Loxodonta africana) ivory to identify population of origin (Vogel et al. 1990, van der Merwe et al. 1990) was exaggerated, because of annual changes in climate that can cause concomitant changes in food-web δ15N and δ13C values in Africa. Although it is true that δ15N and δ13C isoscapes are necessarily problematic in wildlife tracking (e.g. Graves et al. 2002), there are several points that need to be considered in any critique. An isotopic measurement of an organism's tissue represents a time- integrated average of numerous individual feeding events and represents an equilibrium condition between tissue formation and replacement. For blood and muscle tissue, these processes represent periods of perhaps a month in a small passerine (i.e. a period arbitrarily representing 3–4 half-lives or 87–93% of “new” integrated dietary input). Depending on the species, this dietary integration likely represents several hundred feeding events. When we consider a slow-turnover tissue like bone collagen, the stable isotope value will represent many thousands of events. It is the nature of isotopic signal averaging that short-term or low-frequency isotopic variation in food webs is smoothed; so a single isotope value can be very powerful and less prone to stochastic events than generally realized. This is not to suggest that researchers should not be conscious of possible isotopic complexity, but rather that isotopic variation needs to be interpreted in terms of mass balance and the turnover rate of the tissue being examined. At each stage of the annual cycle, the range of isotopic heterogeneity to which a bird is exposed through local food webs will depend on constraints imposed by individual and species feeding ecology and the range or distribution of possible origins for the species. Birds with relatively narrow breeding ranges, such as the Kentucky Warbler (Oporornis formosus), will necessarily involve a narrower range of potential isoscapes than species like Tennessee Warbler (Vermivora peregrina) or Swainson's Thrush (Catharus ustulatus). The same argument applies to considerations of complexities associated with agricultural isotopic heterogeneity that a bird may be exposed to, a factor particularly relevant when using stable-carbon and stable-nitrogen isotopic measurements to delineate origins. Species that are almost exclusively dependent on prey derived from closed- canopy forest, such as the North American wood warblers (Dendroica spp.), will be less influenced than species more associated with agricultural landcapes, such as Red-winged Blackbird (Agelaius phoeniceus; Wassenaar and Hobson 2000). The value of the SIA approach will therefore depend on life-history traits of individual species or species groups, so that blanket statements about whether SIA “works” or does not are meaningless. Recent advances in remote sensing and geographic information systems (GIS) technology are making it possible to combine information layers to derive expected C3 and C4 plant distributions on the basis of averaged climate parameters and knowledge of plant physiology (Still et al. 2003). Additionally, spatially referenced data sets on agricultural crop plantings are also possible. Combined, these sorts of derivations will help to further constrain expected δ13C isoscapes relevant to avian ecology. An example of where δ13C patterns of food webs work at continental scales to define origins of migrant organisms was provided by Hobson et al. (1999a), who defined a combined deuterium (δD) and δ13C isoscape for monarch butterflies (Danaus plexippus) raised on milkweed (Asclepias spp.) throughout their eastern range in North America. Surprisingly, that study showed impressive continental structure in both isotopes, which makes it possible to define natal origins of butterflies with greater resolution than could have been achieved with each isotope singly. Nonetheless, anthropogenic inputs to the isotopic reservoir available to birds can certainly be a cause for concern and will always be a factor to consider in most connectivity scenarios (Alexander et al. 1996). Although ecologists have only recently become aware of patterns of deuterium (δD) in precipitation on various continents and their significance in tracking migratory wildlife (Bowen et al. 2005), the North American growing-season average precipitation (δDp) map is arguably the most isoscape it is the most useful isotopic pattern available to studies of migratory connectivity for terrestrial species. The that of birds have values that the continental pattern of has provided with a very powerful to approximate origins of migrant birds in North and the pattern of in North usually results in strong but weak For species relatively narrow this approach has been powerful et al. Rubenstein et al. Hobson et al. The isotopic relationship is the potential for annual in continental but as with there are certainly potential in the application of this technique and Hobson 2004). The following points will of these questions and for The pattern of deuterium in precipitation continents that the basis of most recent migratory connectivity studies is the of in data by the This was to help the of available throughout the the nature of the data is both in time and so the of these continental patterns is derived from the averaging of the isotopic data and of patterns through spatial or and of the data interpretation are available (e.g. Hobson et al. Bowen et al. 2005), and make it possible to for average precipitation values for (e.g. et al. 2004). with for North is for regions are also difficult to map isotopically, and areas on the of the show high isotopic complexity with the also for the and of in Bowen et al. In regions are to local and to events that can contribute to relatively high in (Hobson 2003). is known to food-web and to using such data are possible et al. 1994). such for the reasonably relationship we see between and for including data sets involving from and a time range (Hobson and Wassenaar Wassenaar and Hobson Kelly et al. see also et al. and is with for typically being as recently by and for a large feather data in North America, there is evidence for differences in the of the relationship between and This suggests that the isotopic discrimination factor linking and to be about at least for and Hobson Hobson et al. may not be to areas of the or for avian and have also recently isotopic variation in of in and considered several of variation the of the technique as with conventional in origins of migratory birds, there are that researchers need to consider when using this The first is that we local values to the values provided by the various continental This is simply the nature of our to a single with a of values using from species of interest is (e.g. Hobson et al. should also the to the data for a location (e.g. and 2005), because we food webs to seasonal patterns in rather than short-term and the nature of the data an average on the of is not and will be or depending on and the isotopic typically in use in North and are based on the growing-season average and analyses to have been between by breeding birds and the value expected from breeding or interested in defining origins of birds wintering on various continents should that such have not been we like to of expected wintering values Mazerolle et al. 2005). This be for large data sets available for North and but it is not how food webs to seasonal changes in of have provided the advances in making migratory but there are of in food webs that contribute to the we issue is that with and nitrogen are relatively weak with those with and a of in any will with This has research of measurements made at where can and Hobson 2003). This is a work in but it should be possible for to a single of and avian tissue values not influenced by it is usually not possible to make direct of data Although the of this is relatively it will change seasonally as The of is the potential for large data sets through A problem with measurements is that from can with tissues (Hobson et al. This is not a problem for species that derive the of their through diet or for those and diet are driven by the same of of very isotopic than the based food will tissues with potentially values. of body in and will result in the of tissue values in birds et al. 2004). If this is not of tissue values in this way to birds at more than their and we are feather data sets in which a small of individuals be reliably on for North because are too (K. A. Hobson and Wassenaar unpubl. data). Species like that periods such as and may have enriched because of of body with those species that molt after the breeding et al. 2003, and 2005). It be that the relationship between and for food webs that are driven by precipitation to and the relationship is expected to there is a significant In in where birds derive from food in driven by from such as and between and are are prone to seasonal changes in values because of interactions between and precipitation Fortunately, patterns of values are available for and and to in the of using measurements for species. Although there is generally an between of and and for relatively to the relationship does not for it is with what the deuterium isotope approach can be used for species using on large for food or or from analysis of there is evidence that the pattern of for North has reasonably for the and climate change may the nature of these patterns toward new the should also be for the of the and in North and the of the North in Although of new to track climate change is not it represents a that will several to In the individual research that are to bird tissue values for known may be to on the basis of the it is that researchers use from or known to have tissues at a known rather than from that may have values because of processes deuterium and or in the et al. 2004). a tissue stable-isotope value with geographic is essentially a problem of In this the stable-isotope field analysis with the field of population et al. there is interest in using and in applications to migratory on knowledge of the expected isotopic distribution in a of interest et al. 2005). than on between and et al. the of using for using isotopic data. an approach is similar to the analyses by et al. (2000) in their approach to evaluate origins of wintering and the study of Wassenaar and Hobson (2000) on Red-winged from North America. et al. and and have raised points that will the way in which we infer origins using isotopic data. the high in by et al. for from single their breeding range in North is because such large isotopic has not been in other geographic areas are too complex of or to apply the stable-isotope technique to infer origins of of feather in species to may involve complex of based et al. have on discrimination in see also et al. 2003, and 2005). recent of development is the of of origins on the basis of information on of birds breeding or wintering the North American can potentially to derived of origin based on differences in species and Rubenstein 2004). the same approach could be used to for birds using the and data the other and Rubenstein not evidence that their approach provided any particularly useful information on for the Warbler because considered such regions of origin with relatively data. For any of it may be more to the isotope data at value and to potential origins using only et al. and make such relatively and can of population origin using or (Hobson et al. 1999, Mazerolle et al. 2005). Nonetheless, are of potential origins based on model and the combined of and spatial are A that to the of individuals to various of origin using only feather values. et al. were the first to consider this For their study on through the that the technique a of of This likely represents an and should be considered the we can do with this single isotope in general the associated with of origin in North depends on of interest et al. and and on how the result in of with more will for in areas of the North American continent. In North America, most that of the in only for that If a deuterium map could be for and for other wintering regions in and the this in the of origin of tissues (e.g. in on wintering For small with will For species that with in (e.g. the of and migrant individuals could be a isotopic map also be of to researchers interested in of species that A useful deuterium isoscape for could be using a of more derived from the isotopic measurement of of species at known Although significant for continental of this can be by constraints of species range and habitat This various spatially data sets, but the of these data sets, both available and to be has not been are available for most as are layers that define agricultural and so on can possible of an passerine by the with regions or a size or from or (e.g. and 2003). The only in the development of this field to be associated with and the or of the spatially has been made using feather that have been and measured for a concern is how feather size from can values (G. J. Bowen and Wassenaar pers. the small for measurements to be a more has to be a study that techniques and the of using or from for need to be using captive birds raised on isotopic diets and to that are not by diet In the same that previous researchers have the relationship between and for terrestrial species, we should the relationship between of species and seasonally average for this be most for North on the basis of the previous of and a map of in derived from the a more analysis of associated with of individuals to origin. In this we to the with which we individuals to origin using values. This is not a the nature of the data but we should see a spatially map for and (G. J. Bowen pers. Similarly, spatial of isotopic to be expected in avian tissues for other isotopes may also be to our interpretation of avian tissue stable-isotope values is our knowledge of the isotopic we because of diet nutritional quality, diet and Although data sets from birds are useful (e.g. and 2005), isotopic and between individuals studies where diet in the case of and can be studies are to data associated with The recent that values et al. is but studies using more studies are that migration using wind and the of dietary such nutritional in the that patterns of isotopic discrimination associated with the of endogenous tissues are the same as those associated with an model (Gauthier et al. have not been the of birds in by eggs isotopic between endogenous tissue and and the same for species that are and are These data will help to seasonal interactions at the of direct from wintering grounds or to breeding grounds and so in an to seasonal interactions to To date, isotopic forensic to track seasonal interactions and movements of birds, and have on the and are known to show isotopic patterns that can be to processes in to regions of continents and between and avian tissue isotope values for several including those of and are (e.g. and et al. 2003). The recent of a of isotopic measurements for not to for this and provided to for the isotopic to track van and Wassenaar provided useful and to For continental biome see