Area Sensitivity in North American Grassland Birds: Patterns and Processes

GRASSLAND BIRDS HAVE declined more than other bird groups in North America in the past 35–40 years (Vickery and Herkert 2001, Sauer et al. 2008), prompting a wide variety of research aimed at understanding these declines, as well as conservation programs trying to reverse the declines (Askins et al. 2007). Area sensitivity, whereby the pattern of a species' occurrence and density increases with patch area (Robbins et al. 1989), has been invoked as an important issue in grassland-bird conservation, and understanding the processes that drive area sensitivity in grassland birds is a major conservation need (Vickery and Herkert 2001). Here, we review the literature on North American grassland bird species that is relevant to the following questions. (1) What is the evidence for area sensitivity in grassland birds? (2) What are the historical explanations for area sensitivity? (3) What ecological processes could produce area sensitivity? (4) How does landscape composition affect our ability to detect area sensitivity? And (5) what are the conservation implications of knowing the processes behind area sensitivity? Because of space limitations, we could not cite every paper we reviewed; the cited papers are given as examples of the literature in this field. “Area sensitivity has been invoked as an important issue in grassland-bird conservation, and understanding the processes… is a major conservation need…. [W]e are interested in aspects of breeding ecology that affect the settling of birds and their use of patches of different sizes… these include territoriality, social information, philopatry, and predation,” Grassland ecosystems originally dominated central North America. Tallgrass prairie in the east graded into mixed-grass prairie and, finally, shortgrass prairie in the west (Samson et al. 1998, Askins et al. 2007). Prairies, in particular the tallgrass prairie, are among the most extensively altered systems in North America, owing to Native American management practices and subsequent settlement and development of agriculture by Europeans (Houston and Schmutz 1999, Higgins et al. 2002, Askins et al. 2007). Currently, smaller and more fragmented patches of planted grasslands dominate the remaining eastern grassland systems (Warner 1994, Askins et al. 2007). These surrogate grasslands are composed of Eurasian grass and forb species, are typically associated with agriculture, and include hay fields, pastures, and fallow and old fields (Sample et al. 2003). In the Great Plains, woody encroachment and agriculture are reducing the area of grasslands, reducing patch size, and increasing edge (Coppedge et al. 2001a, Grant et al. 2004). More recently, even these surrogate grasslands are disappearing (Askins et al. 2007). In the United States, between 1982 and 2003, ∼6 million ha of pasture and ∼4 million ha of rangeland were lost (Natural Resources Conservation Service 2007). Biofuel development that results in the loss of undisturbed grassland is an emerging conservation issue (e.g., Fargione et al. 2008). Area sensitivity is a concept originally introduced by Robbins et al. (1989) for forest birds in the eastern United States, and many researchers have since identified this pattern in other systems, such as shrubsteppe (e.g., Knick and Rotenberry 2002) and grasslands (e.g., Herkert 1994). Clearly, density and frequency of occurrence are closely intertwined: as the density of a species in a habitat patch varies, the frequency of occurrence of that species in sample plots within that patch will covary with it. Because of the close relation between these metrics, area sensitivity can be defined as a positive relationship between either probability of occurrence or species density and area. Area-sensitivity status of North American grassland-obligate birds documented by studies that accounted for passive sampling (updating Johnson 2001). Positive = increased occurrence or density with patch area, negative = decreased occurrence or density with patch area, and variable = both positive and negative relationships of occurrence or density with patch area. Results for which no effect was found are not reported; nonsignificance does not demonstrate a lack of effect. Area-sensitivity status of North American grassland-obligate birds documented by studies that accounted for passive sampling (updating Johnson 2001). Positive = increased occurrence or density with patch area, negative = decreased occurrence or density with patch area, and variable = both positive and negative relationships of occurrence or density with patch area. Results for which no effect was found are not reported; nonsignificance does not demonstrate a lack of effect. Johnson (2001) surveyed the literature on grassland birds to evaluate the evidence for area sensitivity; he tabulated those studies that did not have passive-sampling issues and accounted for habitat differences between survey units. Using those two criteria (i.e., no passive-sampling issues, adjustment for habitat differences), we updated Johnson (2001), focusing on the 32 temperate grassland-obligate birds of North America (Vickery et al. 1999). We considered only studies that entailed collection of bird data (i.e., meta-analyses and those using Breeding Bird Survey data were not included). We also excluded species results for which no effect was found, because a nonsignificant result does not demonstrate a lack of effect. We note that some studies (e.g., Johnson and IgI 2001) were done across large geographic areas, so number of studies for a species does not equate to geographic coverage. Of the 32 species, half have been demonstrated to exhibit area sensitivity in occurrence or density in at least one geographic area (Table 1). Three species (Vesper Sparrow, Le Conte's Sparrow, and Dickcissel; scientific names are given in Table 1) exhibited area sensitivity only in terms of their occurrence, and all showed a positive effect. Two species exhibited area sensitivity only in terms of density; positive area sensitivity was reported for Northern Harrier, whereas variable results were found for Western Meadowlark (Table 1). For the 13 species with both occurrence and density information, positive area sensitivity was consistently reported for both variables for eight species, and negative area sensitivity for one (Brown-headed Cowbird); variable results (for occurrence, density, or both) were found for the other four (Sedge Wren, Savannah Sparrow, Grasshopper Sparrow, and Bobolink) (Table 1). Two points are worthy of note. First, the most recent literature focuses more on species' density relationships with area than on occurrence patterns. This may be attributable to a relatively recent shift in the conservation paradigm from island biogeography to metapopulation theory, with a consequent focus on population size (Hanski and Simberloff 1997). Second, some of the most widely studied species have shown variable responses to area (Table 1). This may suggest that the “consistent” relationships found for some lesser-studied species may not hold up once they are studied in additional geographic areas. When researchers started noticing area sensitivity (e.g., Faaborg et al. 1995), they typically inferred the causal mechanism from island biogeography theory (MacArthur and Wilson 1967). Island biogeography theory was focused on explaining increasing species richness with island size and was based on the idea of a colonization-extirpation balance (i.e., area-per-se; Connor and McCoy 1979). Connor and McCoy (1979) discussed two additional hypotheses to explain the species richness-area relationship: passive sampling and habitat diversity. For each hypothesis, we briefly discuss the background development of the idea and then review the application of the idea to area sensitivity in grassland birds. Passive sampling was proposed by Connor and McCoy (1979) as the null hypothesis for the species richness-area relationship; Connor and McCoy (1979:792–793) proposed that “species number is controlled by passive sampling from the species pool, large areas receiving effectively larger samples than small ones, and ultimately containing more species.” This logic can also be applied to individual species: large patches are more likely to be occupied by a species, by chance, than small patches. Few studies have assessed the plausibility of the passive-sampling hypothesis. Connor and McCoy (1979) suggested that a direct proportionality between immigration rates and area would support the passive-sampling hypothesis, though we know of no study that has looked for this relationship. Instead, studies have focused on species occurrence and resulting species richness based on random sampling from the regional species pool (Haila et al. 1993). See Askins et al. (1990) for passive sampling applied to Neotropical migratory bird Grassland patches are by species be the idea of passive sampling is to the issue of area sensitivity in patches variable sampling patch is to occurrence 2001). When survey large patches with more survey than small patches (e.g., sampling to and not that into in a they can a positive relationship between probability of occurrence within a patch and patch size because of the larger area within large patches et al. Johnson 2001). to for this can to species as area 2001) of they are within the patches. This is more likely to with species at density (i.e., et al. In studies of grassland passive sampling is controlled for in the study (e.g., by areas on all patches of patch or in the (e.g., of areas are for or density is as the variable of More such as for in occurrence among survey within a patch and IgI 2001, are cited in Connor and McCoy proposed as the of area were a result of or habitat with the associated species and, species number with area because of an in the number or of in the applied the hypothesis in a metapopulation the whereby large areas are more than small areas and, may include not found on small areas. would be more species in the large areas because their habitat is more likely to studies of habitat in grassland birds (e.g., Wilson and and 1999, McCoy et al. 2001) have shown that the birds into of suggested that habitat by birds in grasslands is based on and This has to of grassland birds on the of their with the idea that species on a patch a of (e.g., and 1997). produce a pattern of area sensitivity the hypothesis, large grasslands would have a variety of than small patches and, would be more likely to species' habitat This is to in and patterns. as a for area sensitivity has been considered in studies of grassland birds. Instead, researchers for habitat either by or habitat are on the survey and are then in an that patch area (e.g., Herkert 1994, et al. 2002, et al. and 2008). this does not large patches have more habitat than small patches more a species' habitat is more found on large patches. for habitat at the patch habitat such as the of of would need to be among patches. Connor and McCoy (1979) suggested areas of size with different of could be in which of are to have different We know of no grassland-bird study that has the hypothesis as an for of area Herkert showed that may some in bird species' within small hypothesis the by that an of species richness with area is attributable to and rates of species in patches of and McCoy 1979). island biogeography and metapopulation theory (Hanski that larger patches larger patch size and so are likely to by on the ability of species to across a of and the between patches (i.e., of a species from a patch results from or of all that occupied the with a lack of immigration from other patches. idea that to rates on small which is by on island bird (e.g., et al. is to these on birds showed that patches that exhibited between years to be smaller and more from occupied patches than patches that did not exhibit et al. Connor and McCoy (1979) that to the hypothesis from passive decreased rates for large as an be has been done on grassland birds to In the only study to and using Grasshopper found that in small fields of than in large Passive sampling be considered a null that be accounted of area sensitivity are are of the need to for passive though some studies have not this as by Johnson has been done on habitat with patch increased patch size to increased population size is a of both island biogeography and metapopulation theory will to increased density of a given species with increased patch size et al. Here, we some of the ecological processes that affect settling of grassland birds and their use of patches of different which could to density on large patches. (e.g., Connor et al. have discussed focusing on ecological processes to relationships from a and et al. for a focus on processes to area and edge in fragmented We also from of grassland-bird papers that were as explanations for and into (e.g., on the hypothesis are and 1999, and 2004). such as (e.g., and were not because was (e.g., in grassland bird species is or not to and and 2001, We focus on ecological processes that may patch and species' breeding and We briefly background and then discuss the processes in relation to area sensitivity in grassland birds. is as random of at a is that once a of size, they will to from so by and 1999). In breeding likely the patch size, because some area in which to (e.g., 2001). the area are to a breeding demonstrated not understanding size can result in density to the relationship of density and patch area. territoriality, a patch size, is not a for area sensitivity 2001). (e.g., is an important of breeding ecology in birds (e.g., of and of breeding birds in produce a pattern of area sensitivity, habitat be to patch (2001) a to the of in relation to the habitat patch the population density of birds in the and the of only in the patch the density in large patches than in small patches. is some evidence that for are in smaller patches and 1998, et al. can be by the use of social such as social and et al. 2001, 2001, and social is to be in grassland birds et al. et al. In and Faaborg social of in a patch increasing the probability that other will in the and that was an important settlement patterns. Using a et al. found that social has the to the number of occupied patches in a metapopulation of are likely between social in is et al. 2001, and For both social and have been found to affect settlement in the et al. 2004). in has for explaining size and is defined (e.g., and will affect of patch size and area is in grassland birds. Of the species in Table have or and et al. and 1995), Meadowlark 1995), and 1995), and Western Meadowlark and 2008). For the other species, use of the from to not even species on the of birds have areas from areas (e.g., Savannah Sparrow, and and the size of the will be than the area for Because the is typically density will be a in the patch size to be by the in this could to area For Northern have a breeding of ha and in et al. this species on a patch of only In this the birds fields as additional et al. 1999). of area of use (i.e., breeding would area for species that use more than a patch for We know of no grassland-bird study that has this of in relation to area on habitat for grassland birds is and suggested that may to a pattern of area sensitivity in In this the may not be as as the of the patch and birds may with more would have and birds would breeding in resulting in decreased bird in small patches. We know of no grassland-bird study that has habitat with patch are that social may in grassland birds. grassland bird species in or these include Northern Harrier, Sparrow, and (e.g., and and and 2001, Herkert et al. have rates to breeding and are to use social to settling and For in to and in those the of the et al. on a different species, et al. to grassland patches the use of We know of no grassland-bird study that has social affect patterns. the of as an 1995), birds may to small patches because of a in small patches increased rates have to use of small patches could to (e.g., and 1994, et al. that small patches may have been more than that on small and, habitat settling is could then that small patches. of small may be an and grassland birds may large grasslands or with (e.g., In birds may have a to a or of or associated with and of forest birds is than that from has been well documented et al. of is and breeding to their patches and more birds in large patches because is the resulting density will be in large other This result is for frequency of the pattern will more with a frequency of than would with a In a breeding could to a population among is than that for is on in large grassland patches for both et al. 1994, et al. and and and Faaborg 1999, et al. Herkert et al. 2003, and et al. et al. differences in into in small patches for grassland bird species has not been (e.g., and Faaborg found that of was to patch size, this did not result in in small on grassland bird is not attributable to (e.g., and the associated with woody is also a of that in the grassland (e.g., et al. 1999, and and 2003). the of edge in grassland birds is likely an between the of edge the the habitat of the and the species and of grassland For in a grassland the were which were more from in and was for than for those in et al. in pasture habitat with some woody grassland was not by because by both edge and grassland was et al. We are to and their or within grassland patches of different In some areas, the may between small and large patches et al. In may in patches of et al. found that was in small grassland patches. did not small in the of their size and 2003, et al. is what would into small for we lack on in patches of the is that (e.g., small of large may be of grassland bird and breeding on and breeding is because of the of and following the and of In has been found to be in migratory species and Savannah and were the two grassland species in the et al. found rates for and of Savannah Sparrow, Grasshopper Sparrow, and and (1989) documented breeding in both and Savannah and and also have shown with most to the each Breeding to be to individual This has been documented in a grassland bird and found that of that been in the with only for the that did not and (1989) reported that rates of were the were We know of no and breeding in relation to patch the ecological processes discussed have not been as explanations of area sensitivity in grassland birds. research will be to evaluate these may be to to some aspects of of grassland bird has a of may that can be from the landscape patches. with Neotropical migratory birds et al. 1995), a is to the for as well as to affect at the patch et al. 2001, and 2003). landscape of a focus of grassland bird research in the We briefly discuss with a focus on application to area sensitivity in grassland birds. to a landscape into area sensitivity hypotheses is to an ecological et al. that the in which a grassland bird has the landscape as an of habitat in grassland birds. is as a in which birds regional or landscape at a major is of what habitat are with the in which grassland birds habitat (Sample et al. 2003). For birds may areas of grassland habitat of different as a whereas researchers would researchers typically the patch as an area of relatively habitat Because on the of sampling for grassland birds is are to the of the patch as with the is to that composition and of the landscape within (i.e., that from the survey (e.g., et al. 2002) or from the of a patch (e.g., and 2001, and 2008). is no that results of will such may explain the data than based on a For both and Johnson and and found that patch and landscape were in explaining density for most grassland bird species that they may breeding species use patches and, affect aspects of the breeding could produce of area is that grassland birds at et al. to their of woody in the landscape to be associated with and of grassland birds in the patch (Coppedge et al. and et al. and Grant et al. and Johnson et al. and 2008). of grassland habitat in the landscape may also be important for grassland does not to be the landscape issue for grassland birds. grassland bird species to large patches will use small patches that are within a larger grassland et al. et al. Western Meadowlark and and is some evidence that can be an of and rates or density of grassland bird species within the et al. found that rates of both tallgrass and mixed-grass prairie and were in small patches was a large of grassland habitat in the landscape with rates in patches with grassland habitat and found no evidence of a relationship for and Savannah in the were in a landscape with a large of grassland they found a positive relationship the were in with a large of In studies on grassland birds have found that area sensitivity is in composed of a of grassland and 2001, et al. 2002, and and 2008). though landscape variables may explain some in the occurrence and density of some species, explanations for landscape have been proposed for grassland birds et al. 1998, Johnson et al. 2001). For our focus on area sensitivity, landscape may affect the ecological processes we discussed For social may affect species use the landscape and may also be by landscape such as patch could of social on settling patterns. For grassland of size, that are by woody habitat may be likely to be occupied an individual may be likely to such an and social may be likely to can be to was a of habitat for and and For given the of and found to affect grassland a landscape may be to some species affect grassland birds in the For because the large of and typically composition of can be by landscape and et al. 2001, and 2003). is landscape regional processes may be important for understanding their at the patch For found the for grassland birds in prairie patches in a of the were at a area sensitivity of grassland birds in a landscape will be a area of research for some to Knick and Rotenberry for a of these issues for shrubsteppe will be to landscape in the study to either for the effect (e.g., in or to include as an variable in (e.g., grassland patches in patches in grassland also et al. for a to understanding edge and patch area conservation of grassland birds is to management of of using a will to be area sensitivity is an important concept grassland-bird conservation et al. 1998, et al. 2001). What is is landscape will For were to the Bird Conservation Area for grassland bird management in some (Sample and et al. 2003). the a large of undisturbed grassland is in a large of with additional patches of grassland within the most of which are this was as a for management of grassland birds in Because landscape composition and use across the Great and in the and of grasslands and such as and the across will be in may need to be for different et al. the using patches in eastern North and et al. that large areas of tallgrass prairie was they also that the may not be the in the they This result is not given that of area sensitivity in grassland birds are by the results of et study the need for management based on area sensitivity in different between area sensitivity in a patch and the landscape also points to a in conservation that on the concept of area the idea that geographic areas with patches of habitat that are considered for grassland birds are for conservation conservation focus on only large habitat patches may small patches worthy of grassland patches in may conservation for grassland birds (e.g., et al. 2002, et al. In small patches of prairie can be important for or prairie as well as for in and processes are important for management of grassland birds (Askins et al. 2007). focusing on ecological processes also may be important for understanding regional in bird to For knowing edge are more important than grassland in grassland in small patches would be because management for reducing the effect of edge could be different from those for grassland (e.g., for edge proposed by et al. aspects of breeding ecology in relation to patch area can as How many species are the Northern and can use small patches of habitat for breeding in a these species breeding in small this would conservation such as what to or conservation be with to one or to would be of conservation to more or other aspects of social can be to grassland birds into settling in areas. In would be important to know that birds are from habitat to habitat not Grassland ecosystems the have been by and this at an increasing Conservation issues, such as loss of and surrogate grasslands and are likely across these systems (Vickery et al. 1999, 2004). In an increasing number of and development and and the of associated with an increasing population is of particular the of grassland and and, as a our for grassland birds at large landscape and may conservation at smaller as our understanding of the ecological of grassland bird species, area and the relationship between these and of we will be to more effectively to the management and conservation of these Survey 1999, at the of for to discuss to area sensitivity and a regional for this in grassland birds. researchers with in grassland bird ecology one or both of the and In to the of this these were and These were the for this and we the for these We and for of the We and one for their which our We the and for the of the We the of and for with