Habitat specialization explains avian persistence in tidal marshes
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1 Habitat specialization explains avian persistence in tidal marshes Maureen D. Correll, 1, Whitney A. Wiest, 2 Brian J. Olsen, 1 W. Gregory Shriver, 2 Chris S. Elphick, 3 and Thomas P. Hodgman 4 1 School of Biology and Ecology, The University of Maine, Orono, Maine USA 2 Department of Entomology and Wildlife Ecology, The University of Delaware, Newark, Delaware USA 3 Department of Ecology and Evolutionary Biology, Center for Conservation and Biodiversity, University of Connecticut, Storrs, Connecticut USA 4 Maine Department of Inland Fisheries and Wildlife, Bangor, Maine USA Citation: Correll, M. D., W. A. Wiest, B. J. Olsen, W. G. Shriver, C. S. Elphick, and T. P. Hodgman Habitat specialization explains avian persistence in tidal marshes. Ecosphere 7(11):e /ecs Abstract. Habitat specialists are declining at alarming rates worldwide, driving biodiversity loss of the earth s next mass extinction. Specialist organisms maintain smaller functional niches than their generalist counterparts, and tradeoffs exist between these contrasting life history strategies, creating conservation challenges for specialist taxa. There is little work, however, explicitly quantifying specialization ; such information is necessary for the development of focused conservation strategies in light of the rapidly changing landscapes of the modern world. In this study, we tested whether habitat specialism explains the persistence of breeding bird populations in tidal marshes of the northeastern United States. We used the North American Breeding Bird Survey (BBS) together with contemporary marsh bird surveys to develop a Marsh Specialization Index (MSI) for 106 bird species that regularly use tidal marshes during the breeding season. We produced four metrics of species persistence (occupancy, abundance, total biomass supported, and 14- yr population trends) and compared them to MSI values in one of the first community- scale demonstrations of specialist loss in disturbed landscapes. Our results confirm that tidal marsh specialism has short- term benefits but long- term consequences for bird persistence in coastal marsh systems, results that are generalizable across many changing landscapes. We then use this robust support of niche theory to recommend MSI as a tool for quantitatively identifying species of conservation concern in disturbed and rapidly changing landscapes such as tidal marsh. Key words: climate change; niche; specialism; species conservation; tidal marsh. Received 15 December 2015; revised 2 July 2016; accepted 22 July Corresponding Editor: W. A. Boyle. Copyright: 2016 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. maureen.correll@maine.edu Introduction Generalist and specialist life history strategies are fundamental concepts in ecology and can be explained most efficiently through the lens of the ecological niche (Grinnell 1917, Elton 1927, Hutchinson 1957, 1978, Macarthur and Levins 1967, Leibold 1995, Holt 2009). The modern niche concept is defined by the relationship between a group of organisms and their physical (e.g., temperature, precipitation) and biological (e.g., predator interactions, food availability) environment (Shea and Chesson 2002, Chase and Leibold 2003). Any particular point in ecological niche space will describe (1) the environmental requirements of a species to persist (birth rate death rate) and (2) the impacts that a species has upon its external environment at a particular place and time (Leibold 1995, Chesson 2000, Shea and Chesson 2002). Within this theoretical context, specialism is a necessarily relative term where specialist taxa are those with a smaller requirement niche breadth along at least one requirement gradient when compared to 1
2 more generalist taxa (MacArthur 1972, Julliard et al. 2006). The generalist, while able to endure use of a wider breadth of physical environments and biological interactions, cannot exploit any one combination of environmental settings as effectively as their specialist counterparts. In a static environment, natural selection should faithfully favor the path of the specialist, whose competitive advantage (Levins 1968, MacArthur 1972) benefits species persistence in heterogeneous landscapes (Levins 1968, Kawecki 1994). However, there are known negative consequences to being a specialist. Specialists do not exploit novel environments well, and while they are at a competitive advantage at the center of their most specialized requirement axis, they are at a disadvantage outside of this zone compared with both other specialists and generalists. Specialists thus exhibit smaller range and population sizes, and more limited dispersal capabilities (Gaston et al. 1997, Colles et al. 2009) than generalists in the same landscape (Wilson and Yoshimura 1994, Devictor et al. 2008). Environmental setting is therefore integral to determining the fate of generalist vs. specialist species; predictable, unchanging landscapes favor specialists, while fluctuating landscapes favor the persistence of more generalist species (Levins 1968, Devictor et al. 2008). While theoretical tradeoffs between specialism and generalism are well documented, these concepts have not been rigorously quantified across taxa (Holt 2009). Degree of specialism may refer to variation across individuals, species, or functional groups (Bolnick et al. 2003, Blonder et al. 2014), or to different forms of adaptation (e.g., diet vs. habitat specialization). Quantification measures for specialism also vary, are often limited to a few species (Devictor et al. 2010), and are usually applied across multiple habitat types (Jonsen and Fahrig 1997, Julliard et al. 2006, Devictor et al. 2008). Defining and quantifying specialism in the context of particular habitat or ecosystem requirements, with the end goal of using these findings as conservation mechanisms, is the next logical step in the application of these principles to biodiversity conservation. Given the current mass extinction crisis (Barnosky et al. 2011) and fragmentation of global resources through direct and indirect anthropogenic effects (Fischer and Lindenmayer 2007), the outlook is dire for specialists globally (Futuyma and Moreno 1988, Devictor et al. 2010). Worldwide habitat fragmentation may further decrease the persistence of specialist species. Rising global temperature, sea levels, and altered storm frequency and intensity can also create environmental conditions that fluctuate beyond the constrained niches maintained by specialist species. As a result, specialists have been referred to as the great losers of past and current global changes (Devictor et al. 2010), and specialism is now considered one of the dominant factors determining extinction of species (Dennis et al. 2011). Quantification of specialism within a particular habitat type therefore may not only provide a strategy for confirming long- standing theoretical concepts, but also be a potential indicator of overall conservation concern for a species. We explore the persistence of tidal marsh bird species in the northeastern United States as (1) a test of the costs of specialism in degraded, fragmenting landscapes as predicted by niche theory and (2) as a potential rapid assessment mechanism for conservation concern in tidal marsh bird species. These marshes have been used and modified heavily by humans since European colonization for agriculture, mosquito abatement, and ready access to the ocean (Bertness et al. 2002, Silliman and Bertness 2004, Gedan et al. 2009). Further, tidal marshes across the northeastern United States experience rates of sealevel rise roughly twice the global average, with even higher rates recorded within the past 5 yr (Sallenger et al. 2012). This marsh degradation may alter the landscape to the point of deviation from specialist niches, and make them well suited to test hypotheses about species persistence in this scenario. Answering these theoretical questions is also particularly important for conservation planning, as the results will have certain implications for the valuable ecosystem services tidal marshes provide to coastal communities (including biodiversity, Shepard et al. 2011). In this study, we define a measure of specialization to tidal marsh, the Marsh Specialization Index (MSI) for commonly detected species of tidal marsh birds. This index is akin to the Species Specialism Index (SSI) developed by Devictor et al. (2006, 2008) but quantifies specialism relative to a single habitat type. Development of the MSI is intended to both advance the standardized 2
3 quantification of habitat specialization and serve as a tool for identifying species of conservation concern. To accomplish these objectives, we test for tradeoffs across a gradient of specialism between short- term success within the habitat (occupancy, abundance, and biomass) and persistence in the face of habitat change (14- yr population trends). Further, we use existing regional bird conservation assessments (Partners in Flight, or PIF, scores) in northeastern tidal marshes to assess the utility of the MSI as a future rapid assessment tool for the conservation status of tidal marsh species. We expect to see increased short- term success and decreased long- term success with increasing MSI value. Additionally, we expect to see a positive relationship between regional PIF score and MSI value. Methods Developing the Marsh Specialization Index (MSI) We conducted contemporary bird surveys at 1770 locations during the summers of between coastal Maine and Virginia (Appendix S1). These survey sites were selected using a Generalized Random Tessellation Stratified (GRTS) sampling scheme as described in Wiest et al. (2016). Each survey location was visited two to three times each year between 15 April and 31 July, with smaller, shifting survey windows within each state to account for differences in local phenology. All surveys were completed between sunrise and 11 a.m. by observers proficient in visual and aural identification of tidal marsh birds; technicians were trained through a standardized process at the beginning of the field season and supervised throughout to maintain consistency. When possible, we revisited locations from historical bird surveys during data collection (n = 457). These historical locations were spread across all states in the survey region, although more were located in New England (Maine to Connecticut, n = 265) than the Mid- Atlantic (New York to Virginia, n = 192). Surveys consisted of a 5- min passive point count during which we recorded all birds observed using marsh habitat. We also recorded time of detection as well as the distance of each bird from the observer using distance band categories (0 50 m, m, >100 m). Our sampling scheme is fully described in the study by Wiest et al. (2016). We identified the most commonly detected species in northeastern U.S. tidal marshes by scree plot (n = 106) of species relative abundance during the 2012 survey season. To quantify tidal marsh specialization for these species, we then compared these relative abundance estimates in tidal marsh from 2012 to relative abundance in terrestrial systems as measured by the North American Breeding Bird Survey (BBS, Sauer et al. 2015). The BBS is a long- running, continental monitoring program comprised of 3- min point counts within a 400- m detection radius conducted along a series of predetermined, roadside survey routes. For each species, we summed count data across all BBS routes where the route center point was within 100 km of the coastline across our survey region. We corrected for effort by dividing the BBS sum by the number of routes (n = 170) and number of count stops on each route (n = 50). Likewise, we summed our count data from tidal marshes for each species, using detections recorded during the first 3 min of each survey at an unlimited detection radius at each survey point. Again, we corrected for effort by dividing the sum of all individuals counted by the number of total visits across all point counts in To produce our index of specialization for each species, we divided tidal marsh relative abundance by the sum of tidal marsh and terrestrial (BBS) relative abundance. This produces an index for each species (MSI) quantifying its degree of habitat specialization to tidal marsh, with values ranging from 0 (terrestrial specialist) to 1 (tidal marsh specialist) with habitat generalists occurring at intermediate values between these two extremes. This index assumes equal detection probability for each species across habitats and equates 400 m radius counts (BBS data) with unlimited radius counts (tidal marsh data). These detection distances are likely equivalent, as detection and identification of birds to species >400 m from an observer are extremely rare (Emlen 1971). Species metrics Once we calculated MSI for all 106 species, we selected a subset of species for all further analyses that (1) used northeastern tidal marshes during their breeding season, (2) occurred with enough evenness and regularity across our study 3
4 area to withstand a robust trend analysis, and (3) had MSI values of >0.5 to explore the gradient of habitat generalism (MSI ~0.5) to tidal marsh specialism (MSI ~1.0). We excluded beach- and platform- nesting species from this analysis because their abundance in tidal marshes is likely tied to proximity of adequate breeding habitat, and not quality of the tidal marsh habitat that they were using when detected. Occupancy, abundance and biomass We modeled probability of occupancy and abundance of tidal marsh birds in northeastern U.S. coastal marshes using N- mixture models (Royle 2004) in a likelihood framework using the package unmarked (Fiske and Chandler 2011) in R (R Core Team 2015). We used our regional survey data from 2012 to produce these estimates. We used the function occu to estimate mean probability of occupancy and pcount to estimate mean abundance across all surveyed points. We used observation- level covariates of Julian day, time of day, and tidal stage to account for differences in detection probability across visits. For each species, we only included survey sites within a species published breeding range (Cornell Lab of Ornithology 2015). We calculated confidence intervals for these estimates using the Wald approximation function. Estimates of occupancy and abundance apply to the area of marsh contained within a 100 m radius circle (31,416 m 2 ). To estimate average biomass supported, we recorded average adult biomass for each species using Cornell Lab of Ornithology s (2015) estimates for each species and used the mean when multiple mass estimates were given for a species (i.e., across sexes or subspecies). For Nelson s sparrow (Ammodramus nelsoni) and saltmarsh sparrow (A. caudacutus), we used estimates from more recent work on these two species along the Atlantic coast (Ruskin 2015). We then took the product of the average biomass and the point abundance estimate for each species to produce a value for average biomass supported. Population trends We combined our regional survey data from 2011 to 2012 with a historical database of point counts (n = 1550 additional survey points) conducted in tidal marshes from Maine to Virginia, spanning the years following Correll et al. (2016) to generate 14- yr population trends for each species. The resulting database contains records of birds observed using tidal marsh during a passive 5- min point count conducted between sunrise and 11:00 h between 1 April and 1 August of the survey year. The vast majority of historical data have records for both 50 and 100 m radii (n = 2782 points); however, due to differing distance sampling methodologies, a small number of observations were limited to 100- m (n = 93) distance bands, making the databases with which we generated population trends at the 50 and 100- m scales slightly different from one another, although both databases were similar in spatial spread across the survey region. Both historical databases contained observational data from many more survey locations in New England states than states in the Mid- Atlantic. Thus, the population trends reported here could amplify patterns in the north and underplay existing patterns in the south. While other studies using this historical data set find similar trends in tidal marsh species when spatially stratifying their analysis by region ( 2016), our findings should still be considered with a northern data bias in mind. See Appendix S2 for additional detail. We modeled population change using generalized fixed- effect models (GLM) in a likelihood framework in R (R Core Team 2015). In all analyses, we only used survey points that overlapped the Estuarine Intertidal Emergent Wetland layer of the National Wetlands Inventory (NWI) and were within the published breeding range for each species (Cornell Lab of Ornithology 2015). We modeled regional population trends for each species following model structure and fit assessment described in (2016). We used 50 or 100- m distance band detections to produce population trends depending upon the natural history of each species. See Appendix S3 for additional detail. Conservation status We investigated conservation status information for each of the 22 species through review of the Partners in Flight (PIF) combined concern score for landbirds in Bird Conservation Region (BCR) 30 (Partners in Flight Science Committee 2012). This physiographic region covers from coastal Maine to Virginia, nearly equivalent to 4
5 our focal area for this study. These scores were produced in 2012 and are the most up- to- date assessment of regional conservation need for coastal landbirds in the northeastern United States. Of the 22 species, 13 are landbirds and were assigned scores in the 2012 BCR 30 database. As the 2012 PIF scores exclude waterbird species, we also reviewed the Priority Species Pools generated for the physiographic areas of Northern New England (Area 27: Hodgman and Rosenberg 2000), Southern New England (Area 09: Dettmers and Rosenberg 2000), and the Mid- Atlantic (Area 44: Watts 1999), which together make up our focal area for this study. These species scores were generated in the mid- 1990s, but are the most recent quantitative assessment of species conservation concern inclusive of waterbird species. Of the 22 species meeting our criteria, 11 were assigned PIF prioritization scores in at least one of the physiographic region plans. When a species was listed and ranked in a priority species pool for more than one physiographic area, we used the mean of the scores across all areas as a combined score for that species. In both the 2012 and earlier assessments, the PIF prioritization plan (Carter et al. 2000) combines assessments of breeding and nonbreeding distributions, relative abundance, and population trends to assign a single conservation score for each species in relation to that physiographic area. Analyses We tested for relationships individually between the degree of specialization (MSI) and each of the four metrics of species success and persistence (probability of occupancy, abundance, biomass supported, and population trend) using linear mixed- effects models in a likelihood framework using the package lme4 (Bates et al. 2015). We also explored the relationship between MSI and the combined PIF score in a similar model framework to compare assessments of conservation need. To meet assumptions of normality, we first log- transformed two of the five dependent variables (abundance, and biomass supported) and used a logit transformation on probability of occupancy values. To control for the effects of phylogeny, we included taxonomic family as a random effect in all models. This taxonomic grouping accounts for phylogenetic similarities between species but still allows for some variation across these groups. We tested for the effect of specialization by comparing all models to the intercept- only model, and models with a difference in Akaike s information criterion for small sample sizes (ΔAICc) 2.0 were considered equivalent (Burnham and Anderson 2002). We used both fixed and random effects to calculate degrees of freedom for AICc values. We further assessed GLMM model fit using marginal R 2 values using the R package MuMIn (Barton 2015). We used linear mixed- effects quantile regressions in a likelihood framework using the lqmm package (Geraci 2014) to further explore the relationship between degree of specialism and biomass supported. We compared models with τ ranging from 0.1 to 0.9 in 0.1 increments to models with τ = 0.5 (equivalent to linear regression). We again assessed relative model performance with AICc values. Results MSI values Across the 106 species, MSI values ranged from 0.01 (tufted titmouse, Baeolophus bicolor) to 1.00 (saltmarsh sparrow and others, see Appendix S4). We identified 22 species that fit species selection criteria (Fig. 1). Probability of occupancy point estimates (reported with 95% CIs) ranged from 0.02 (0.01, 0.03) for the alder flycatcher (Empidonax alnorum, Table 1) to 0.70 (0.68, 0.72) for the red- winged blackbird (Agelaius phoeniceus). Point abundance estimates for each of the selected species ranged from 0.3 individuals (0.01, 6.4) for the alder flycatcher to individuals (18.25, 21.85) for the red- winged blackbird. The mean biomass supported at each survey point ranged from 4 g (0, 9) for the alder flycatcher to 1593 g (1246, 2035) for the clapper rail. Population trend parameter estimates ranged from 0.43 ( 0.56, 0.31) for the saltmarsh sparrow to 0.61 (0.47, 0.75) for the yellow warbler (Setophaga petechia). Analysis of species persistence We found a negative linear relationship between long- term success in tidal marshes (population trend parameter estimate) and marsh habitat specialism (MSI, Table 2, Fig. 2). Negative parameter estimates occurred, on average, when MSI 5
6 Fig. 1. Sliding scale of tidal marsh specialization represented through a Marsh Specialization Index (MSI), a quotient of the amount of tidal marsh detections vs. total species detections in a combined database of North American Breeding Bird Survey records and tidal marsh bird surveys conducted in We found a positive linear relationship between one metric of short- term success (biomass supported) and MSI (Fig. 2c, dotted line). We found no relationship between either point occupancy or abundance and MSI value. MSI and regional PIF score were also positively related using 2012 landbird and physiographic region PIF scores (Fig. 3; Appendix S5). We found improved fit between biomass supported and MSI value using quantile regression where τ 0.8 (Fig. 2c, dashed line). Model fit was not improved for population trend by varying τ from 0.5. Discussion Habitat specialists in a rapidly changing landscape Tradeoffs exist between specialist and generalist life history strategies. One result of these tradeoffs is that specialists are predicted to reach higher densities than generalists within their defined niche space (Dennis et al. 2011), but habitat generalists are predicted to outperform specialists when these landscapes are degraded or fragmented to the point of divergence from specialist environmental requirements. In our study of tidal marsh birds in the northeastern United States, we found empirical support for the negative consequences of specialism in changing landscapes as predicted by niche theory. In our analyses, we found a negative relationship between population trend and MSI (Fig. 2d), indicating the more specialized a species is to tidal marsh habitat, the less likely it is to persist in this ecosystem over time. When we examined this pattern across each avian family individually (Appendix S6), we found that species with higher MSI values had lower population trends in five (Anatidae, Rallidae, Hirundinidae, Emberizidae, and Icteridae) of the seven avian families examined (not Ardeidae or Parulidae), suggesting that no one family was driving the larger pattern. Additionally, the biomass supported at a survey point for a given species was positively related to MSI value (Fig. 2c), indicating that specialized species have the ability to support larger amounts of biomass per unit of marsh than of their generalist counterparts. This relationship was quantile rather than linear in nature, indicating specialism was a constraining factor instead of a linear predictor of the overall biomass supported by a particular species. Simply put, specialists in tidal marsh had the option of maintaining low or high amounts of biomass, while generalists were limited in the biomass they can support. These findings are consistent with the hypothesis that generalists are limited by their 6
7 Table 1. Specialization and persistence metrics for 22 bird species occurring in tidal marsh between Maine and Virginia (for the remaining 84 species calculated, see Appendix S4). Common name Family Individual biomass (g) MSI Point abundance Probability of occupancy Biomass supported (g) Trend Saltmarsh sparrow Emberizidae (3.24, 5.58) Nelson s sparrow Emberizidae (1.16, 3.2) Seaside sparrow Emberizidae (4.95, 7.58) Marsh wren Troglodytidae (4.46, 7.49) Clapper rail Rallidae (4.45, 7.27) Willet Scolopacidae (5.08, 6.91) Snowy egret Ardeidae (1.18, 1.79) American black Anatidae duck (0.43, 1.35) Great egret Ardeidae (1.41, 2.21) Virginia rail Rallidae (0.09, 3.38) Boat- tailed grackle Icteridae (1.06, 1.93) Glossy ibis Threskiornithidae (0.9, 1.73) Red- winged Icteridae blackbird (18.25, 21.85) Mallard Anatidae (0.7, 1.13) Tree swallow Hirundinidae (3.73, 5.09) Great blue heron Ardeidae (0.84, 2.93) Savannah sparrow Emberizidae (0.25, 2.07) Song sparrow Emberizidae (2.76, 6.41) Yellow warbler Parulidae (2.46, 7.4) Barn swallow Hirundinidae (6.52, 8.54) Alder flycatcher Tyrannidae (0.01, 6.4) Common Parulidae yellowthroat (4.66, 11.92) 0.22 (0.2, 0.25) 0.09 (0.08, 0.1) 0.28 (0.26, 0.3) 0.26 (0.24, 0.29) 0.26 (0.24, 0.28) 0.36 (0.33, 0.38) 0.22 (0.18, 0.27) 0.06 (0.04, 0.08) 0.24 (0.21, 0.27) 0.03 (0.02, 0.05) 0.1 (0.09, 0.12) 0.08 (0.07, 0.11) 0.7 (0.68, 0.72) 0.13 (0.11, 0.16) 0.33 (0.3, 0.36) 0.17 (0.09, 0.28) 0.04 (0.03, 0.05) 0.49 (0.46, 0.51) 0.2 (0.18, 0.22) 0.43 (0.41, 0.46) 0.02 (0.01, 0.03) 0.37 (0.34, 0.39) 83 (64, 110) 33 (20, 55) 148 (120, 183) 71 (54, 91) 1592 (1246, 2035) 1406 (1206, 1638) 535 (434, 659) 916 (519, 1619) 836 (668, 1047) 45 (7, 278) 218 (162, 294) 813 (586, 1126) 1078 (985, 1180) 1023 (805, 1298) 85 (73, 99) 334 (179, 622) 14 (5, 41) 102 (67, 155) 42 (24, 73) 140 (122, 160) 4 (0, 86) 75 (47, 120) 0.43 ( 0.56, 0.31) 0.21 ( 0.33, 0.08) 0.05 ( 0.21, 0.3) 0.07 ( 0.33, 0.17) 0.34 ( 0.61, 0.06) 0.13 ( 0.01, 0.27) 0.11 ( 0.25, 0.02) 0.04 ( 0.21, 0.29) 0.26 (0.12, 0.41) 0.23 ( 0.32, 0.88) 0.21 ( 0.68, 0.25) 0.49 (0.22, 0.76) 0.34 (0.27, 0.41) 0.39 (0.19, 0.59) 0.02 ( 0.11, 0.15) 0.09 ( 0.25, 0.06) 0.02 ( 0.27, 0.31) 0.1 (0.03, 0.18) 0.61 (0.47, 0.75) 0.24 (0.13, 0.34) 0.35 ( 0.13, 0.92) 0.38 (0.29, 0.47) Note: Parentheses contain 95% CIs. ability to efficiently exploit any one particular environment, while specialists are not. These two main findings quantitatively support the dark future generally predicted for habitat specialists worldwide. As ecosystems are fragmented and our global climate changes at rates unprecedented within recent geological history (Urban 2015), habitat specialists reliant upon predictability of a single habitat type will be outcompeted by generalists. This pattern has previously been demonstrated in single- species studies quantifying the declines of specialists worldwide (Clavel et al. 2011); however, our findings provide robust empirical support for these theoretical predictions at the community level across a suite of tidal marsh bird species. 7
8 Table 2. Model results comparing metrics of species persistence in tidal marshes to Marsh Specialization Index (MSI) using linear mixed- effects model (LMM) and linear quantile mixed- effects model (LQMM). Metric Model type MSI β estimate (CI) ΔAICc Marginal R 2 Abundance LMM 0.00 ( 1.57, 1.56) 0.64 <0.01 Occupancy LMM 0.03 ( 1.57, 1.56) 1.19 <0.01 Biomass supported LMM 2.37 (0.4, 4.34) Biomass supported LQMM 2.92 (1.2, 4.64) 5.25 NA Trend LMM 0.94 ( 1.69, 0.19) Partners in Flight (PIF) score LMM 3.7 (0.51, 6.9) Conservation implications These results have potential for immediate application in the conservation world. We found that PIF prioritization score, one of the cornerstone methods for assessing conservation priorities of North American birds, was positively related to MSI value. The more specialized a bird was to tidal marsh, the higher it was prioritized using the PIF assessment method. The species with the highest MSI value in our study, the saltmarsh sparrow, experienced the most severe negative population trend of all species we examined, and occupies a very limited global breeding range completely within our study region (Cornell Lab of Ornithology 2015, Wiest 2015). Extinction within the century is predicted for this species using several different population metrics ( 2016), and it is the highest listed priority species in all three of the PIF physiographic areas in its breeding range. The saltmarsh sparrow is also recognized by the North American Bird Conservation Initiative (Rosenberg et al. 2014), the International Union for Conservation of Nature (IUCN 2013), and multiple state agencies as a species of conservation concern. The saltmarsh sparrow, however, is one of the most studied tidal marsh birds in the northeast; similarly rich demographic information does not exist for many of the other 105 species investigated in this paper. The MSI allowed us to identify this species as a high conservation priority with much less a priori information than those used by past conservation lists, and could be used as a rapid assessment metric with which to identify species of conservation concern in a much more timely and easily repeatable fashion. Use of the MSI in this instance as a rapid assessment conservation metric allows for a real- time assessment of conservation need. The only requirement is adequate survey data both within the habitat of interest and the broader landscape that includes many other habitat types. Given those constraints, it has potential for quantifying specialization and therefore conservation risk on suites of species across taxa on similar landscape- scale databases (e.g., plants of the Western Hemisphere, Enquist and Boyle 2012; Lepidoptera of North America, Lotts and Naberhaus 2016; birds of the western United States, RMBO 2014; reptiles and amphibians of western Europe, Wilkinson and Arnell 2012). As with any index, there are limitations to the MSI values we calculate here. For example, the marsh wren (Cistothorus palustris), which uses freshwater, brackish, and saltwater marshes during the breeding season (Kroodsma and Verner 2014), received a higher MSI value than the willet (Tringa semipalmata) and clapper rail (Rallus crepitans), both ordinarily accepted to be tidal marsh specialist species (Shriver et al. 2004, Wiest 2015). As the accuracy of our approach relies on how thoroughly the reference survey (BBS in this case) samples all potential habitats, any species that uses habitat that is not well represented on roadside routes (i.e., coastal marsh, Sauer et al. 2015) will be assigned a more specialist- biased MSI value. Rare species could also be assigned biased MSI values if their rarity led to sampling errors across habitats that do not reflect their true distribution. For example, the black rail (Laterallus jamaicencis) regularly inhabits tidal marshes of the northeast, but is detected in very low numbers (Wiest 2015), restricting robust analysis of their population status. Black rail was so rarely detected during both tidal marsh and BBS surveys that the species evaded assignment of an MSI value completely. We recommend that these MSI values be interpreted in conjunction with knowledge of 8
9 Logit(prob. of occupancy) A Point abundance B Log (biomass supported) C D Trend parameter estimate MSI Fig. 2. Linear mixed- effects model results comparing Marsh Specialism Index (MSI) for 22 tidal marsh bird species with (A) logit transformation of probability of occupancy (Rm 2 < 0.01), (B) log transformation of point abundance (Rm 2 < 0.01), (C) log transformation of mean biomass supported (dotted line indicates τ = 0.5, dashed line indicates τ = 0.8, Rm 2 = 0.21), and (D) populations trends (Rm 2 = 0.22). Gray shading indicates negative parameter space in panel (D); error bars indicate 95% CIs. 9
10 Saltmarsh sparrow 20 Seaside sparrow PIF combined score BCR Common yellowthroat Barn swallow Song sparrow Tree swallow Boat-tailed grackle Marsh wren sparrow Red-winged blackbird Yellow warbler Savannah sparrow MSI Fig. 3. Linear mixed- effects model results comparing 2012 Partners in Flight (PIF) combined concern scores for Bird Conservation Region 30 for 13 tidal marsh bird species and Marsh Specialism Index (MSI, Rm 2 = 0.31). both the natural history of each species and the strengths and weaknesses of the surveys used to calculate the MSI in order to identify potential outliers in this approach. In an era of accelerated global change, the specialist decline predicted by niche theory in unstable landscapes is apparent in tidal marshes of the northeastern United States. We find that degree of specialism increases short- term success (total biomass supported) and long- term extinction risk (negative population trends), and also find that MSI is positively related to PIF prioritization score in coastal marsh birds. This presents both a quantitative demonstration of theoretical principles at a community level and a promising technique for real- time assessment of conservation concern in tidal marsh bird species and others. When used in conjunction with traditional species assessments, MSI and similar indices will be useful for developing conservation plans to limit the further degradation of global biodiversity loss. Acknowledgments We received primary funding through a Competitive State Wildlife Grant (U2-5- r- 1) via Federal Aid in Sportfish and Wildlife Restoration to the States of Delaware, Maryland, Connecticut, and Maine. Additional funding was provided through a National Science Foundation Integrated Graduate Education and Research Traineeship (DGE ), the United States Fish and Wildlife Service (P11AT00245, G004A), the United States Department of Agriculture (ME0- H ), and the Maine Association of Wetland Scientists. This is Maine Agricultural and Forest Experiment Station Publication Number #3491. We thank the Maine Department of Inland Fisheries and Wildlife, University of Delaware, Rachel Carson National Wildlife Refuge (NWR), Parker River NWR, Monomoy NWR, Bombay Hook NWR, Massachusetts 10
11 Audubon, New Hampshire Audubon, Audubon New York, New Jersey Audubon, The Meadowlands Field Commission, the Smithsonian Institution, SHARP field crews and landowners for data contributions, land access, and field support. Thank you also to J.C. Avise (barn swallow), L. Blumin, J. Taggert (song sparrow), M. Eising (American black duck), M. Baird (Virginia rail), J. Wolf (great egret), D. Berganza (clapper rail), D. Pancamo (common yellowthroat), F. Schulenberg (snowy egret), A. Reago (Nelson s sparrow), M. Baird (Virginia rail), Wikimedia Creative Commons, Clipart- Finder.com, Photogra phicclipart.com, and Cliparts.co for providing images of focal species for use in our figures. We also thank E. Adams and D. Rosco for support during analysis and two anonymous reviewers whose suggestions greatly improved earlier versions of this manuscript. The findings and conclusions in this article are those of the authors and do not necessarily represent the views of our sponsors. Literature Cited Barnosky, A. D., et al Has the Earth s sixth mass extinction already arrived? Nature 471: Barton, K MuMIn: multi-model inference. R package version org/package=mumin Bates, D., M. Maechler, B. Bolker, and S. Walker lme4: linear and mixed effects models using Eigen and S4. Journal of Statistical Software 67:1 48. Bertness, M. D., P. J. Ewanchuk, and B. R. Silliman Anthropogenic modification of New England salt marsh landscapes. Proceedings of the National Academy of Sciences USA 99: Blonder, B., C. Lamanna, C. Violle, and B. J. Enquist The n- dimensional hypervolume. Global Ecology and Biogeography 23: Bolnick, D. I., R. Svanbäck, J. A. Fordyce, L. H. Yang, J. M. Davis, C. D. Hulsey, and M. L. Forister The ecology of individuals: incidence and implications of individual specialization. American Naturalist 161:1 28. Burnham, K. P., and D. R. Anderson Model selection and multimodel inference: a practical information-theoretic approach. Ecological Modelling. Springer Science & Business Media, New York, New York, USA. Carter, M. F., W. C. Hunter, D. N. Pashley, and K. V. Rosenberg Setting conservation priorities for landbirds in the United States: the Partners in Flight approach. Auk 117:541. Chase, J., and M. Leibold Ecological niches: linking classical and contemporary approaches. The University of Chicago Press, Chicago, Illinois, USA. Chesson, P Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31: Clavel, J., R. Julliard, and V. Devictor Worldwide decline of specialist species: Toward a global functional homogenization? Frontiers in Ecology and the Environment 9: Colles, A., L. H. Liow, and A. Prinzing Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches. Ecology Letters 12: Cornell Lab of Ornithology The Birds of North America Online. Correll, M. D., W. A. Wiest, T. P. Hodgman, W. G. Shriver, C. S. Elphick, B. J. McGill, K. O Brien, and B. J. Olsen Predictors of specialist avifaunal decline in coastal marshes. Conservation Biology, in press. Dennis, R. L. H., L. Dapporto, S. Fattorini, and L. M. Cook The generalism- specialism debate: the role of generalists in the life and death of species. Biological Journal of the Linnean Society 104: Dettmers, R., and K. Rosenberg Partners in Flight conservation plan physiographic area 09: southern New England. Program Report. Partners in Flight, American Bird Conservancy, The Plains, Virginia, USA. Devictor, V., J. Clavel, R. Julliard, S. Lavergne, D. Mouillot, W. Thuiller, P. Venail, S. Villéger, and N. Mouquet Defining and measuring ecological specialization. Journal of Applied Ecology 47: Devictor, V., R. Julliard, and F. Jiguet Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos 117: Elton, C. S Animal ecology. The University of Chicago Press, Chicago, Illinois, USA. Emlen, J. T Population densities of bird derived from transect counts. Auk 88: Enquist, B., and B. Boyle SALVIAS the SALVIAS vegetation inventory database. Biodiversity Ecology 4:288. Fischer, J., and D. Lindenmayer Landscape modification and habitat fragmentation: a synthesis. Global Ecology and Biogeography 16: Fiske, I., and R. Chandler unmarked: an r package for fitting hierarchical models of wildlife occurrence and abundance. Journal of Statistical Software 43:1 23. Futuyma, D. J., and G. Moreno The evolution of ecological specialization. Annual Review of Ecology and Systematics 19: Gaston, K. J., T. M. Blackburn, and J. H. Lawton Interspecific abundance- range size relationships: 11
12 an appraisal of mechanisms. Journal of Animal Ecology 66: Gedan, K. B., B. R. Silliman, and M. D. Bertness Centuries of human- driven change in salt marsh ecosystems. Annual Review of Marine Science 1: Geraci, M Linear Quantile Mixed Models: the lqmm package for laplace quantile regression. Journal of Statistical Software 57:1 29. Grinnell, J The niche- relationships of the California thrasher. Auk 34: Hodgman, T., and K. Rosenberg Partners in Flight conservation plan physiographic area 27: northern New England. Program Report. American Bird Conservancy, The Plains, Virginia, USA. Holt, R. D Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives. Proceeding of the National Academy of Sciences USA 106(Suppl.): Hutchinson, G Concluding remarks. Cold Spring Harbor Symposia on Quantitative Biology 22: Hutchinson, G An introduction to population ecology. Yale University Press, New Haven, Connecticut, USA. IUCN IUCN Red List. International Union of Concerned Naturalists (IUCN), Gland, Switzerland. Jonsen, I. D., and L. Fahrig Response of generalist and specialist insect herbivores to landscape spatial structure. Landscape Ecology 12: Julliard, R., J. Clavel, V. Devictor, F. Jiguet, and D. Couvet Spatial segregation of specialists and generalists in bird communities. Ecology Letters 9: Kawecki, T Accumulation of deleterious mutations and the evolutionary cost of being a generalist. American Naturalist 144: Kroodsma, D. E., and J. Verner Marsh Wren ( Cistothorus palustris). In A. Poole, editor. The Birds of North America online. Cornell Lab of Ornithology, Ithaca, New York, USA. Leibold, M. A The niche concept revisited: mechanistic models and community context. Ecology 76: Levins, R Evolution in changing environments: some theoretical explorations. Second edition. Princeton University Press, Princeton, New Jersey, USA. Lotts, K., and T. Naberhaus Butterflies and Moths of North America. andmoths.org/ MacArthur, R. H Geographical ecology: patterns in the distribution of species. Princeton University Press, Princeton, New Jersey, USA. Macarthur, R., and R. Levins The limiting similarity, convergence, and divergence of coexisting species. American Naturalist 101: Partners in Flight Science Committee Species Assessment Database. Version org/pifassessment R Core Team R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. org/ RMBO Integrated Monitoring in Bird Conservation Regions (IMBCR): 2014 field season report. Rocky Mountain Bird Observatory, Fort Collins, Colorado, USA. Rosenberg, K., et al The State of the Birds 2014 Watch List. North American Bird Conservation Initiative, U.S. Committee, Washington, D.C., USA. Royle, J. A N- mixture models for estimating from spatially replicated counts. Biometrics 60: Ruskin, K Investigating sharp-tailed sparrow reproductive biology in an ecological and adaptive framework. Dissertation. University of Maine, Orono, Maine, USA. Sallenger, A. H., K. S. Doran, and P. Howd Hotspot of accelerated sea- level rise on the Atlantic coast of North America. Nature Climate Change 2: Sauer, J., J. Hines, J. Fallon, K. Pardieck, D. J. Ziolowski, and W. Link The North American Breeding Bird Survey (BSS), results and analysis USGS Patuxent Wildlife Research Center, Laurel, Maryland, USA. Shea, K., and P. Chesson Community ecology theory as a framework for biological invasions. Trends in Ecology and Evolution 17: Shepard, C. C., C. M. Crain, and M. W. Beck The protective role of coastal marshes: a systematic review and meta- analysis. PLoS ONE 6:1 11. Shriver, W. G., T. P. Hodgman, J. P. Gibbs, and P. D. Vickery Landscape context influences salt marsh bird diversity and area requirements in New England. Biological Conservation 119: Silliman, B. R., and M. D. Bertness Shoreline development drives invasion of Phragmites australis and the loss of plant diversity on New England salt marshes. Conservation Biology 18: Urban, M. C Accelerating extinction risk from climate change. Science 348: Watts, B Partners in Flight conservation plan: physiographic area 44: the Mid-Atlantic coastal 12
13 plain. Program Report. College of William and Mary & Virginia Commonwealth University, Williamsburg, Virginia, USA. Wiest, W Tidal marsh bird conservation in the Northeast, USA. Dissertation. University of Delaware, Newark, Delaware, USA. Wiest, W. A., M. D. Correll, B. J. Olsen, C. S. Elphick, T. P. Hodgman, D. R. Curson, and W. G. Shriver Population estimates for tidal marsh birds of high conservation concern in the northeastern USA from a design- based survey. Condor 118: Wilkinson, J. W., and A. P. Arnell National Amphibian and Reptile Recording Scheme Report : establishing the baseline. Program report. Amphibian and Reptile Conservation, Bournemouth, Dorset, UK. Wilson, D., and J. Yoshimura On the coexistence of specialists and generalists. American Naturalist 144: Supporting Information Additional Supporting Information may be found online at: ecs2.1506/full 13
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