avian assemblages in the lower missouri river floodplain

WETLANDS, Vol. 29, No. 2, June 2009, pp. 552–562 ’ 2009, The Society of Wetland Scientists

AVIAN ASSEMBLAGES IN THE LOWER MISSOURI RIVER FLOODPLAIN Wayne E. Thogmartin1, Maureen Gallagher2,3, Neal Young2,4, Jason J. Rohweder1, Frank Durbian5, and Melinda G. Knutson1,6 1 United States Geological Survey Upper Midwest Environmental Sciences Center 2630 Fanta Reed Road, La Crosse, Wisconsin, USA 54603 E-mail: [email protected] 2

United States Fish and Wildlife Service Big Muddy National Fish and Wildlife Refuge 4200 New Haven Road, Columbia, Missouri, USA 65201 3

United States Fish and Wildlife Service National Fish Habitat Action Plan 800 University Ave., Maryville, Missouri, USA 64468 4

Natural Resources Conservation Service 727 E PCA Road, Warrensburg, Missouri, USA 64093 5

United States Fish and Wildlife Service Squaw Creek National Wildlife Refuge P.O. Box 158, Mound City, Missouri, USA 64470

6

United States Fish and Wildlife Service Regions 3 and 5 Biological Monitoring Team 2630 Fanta Reed Road, La Crosse, Wisconsin, USA 54603

Abstract: Floodplain habitat provides important migration and breeding habitat for birds in the midwestern United States. However, few studies have examined how the avian assemblage changes with different stages of floodplain forest succession in the midwestern United States. In spring and summer from 2002 to 2004, we conducted 839 point counts in wet prairie/forbs fields, 547 point counts in early successional forests, and 434 point counts in mature forests to describe the migrating and breeding bird assemblage in the lower Missouri River floodplain. We recorded 131, 121, and 141 species in the three respective habitats, a number higher than most locations in the midwestern United States and comprising . 15% of all avian species in North America. Avian species diversity generally increased from west to east along the river, differed among land cover classes, but overlapped between seasons (migration and breeding) and years. Wet prairies were particularly important for conservation as there were 20 species of high conservation concern observed, including Dickcissels (Spiza americana). Important species for monitoring biotic integrity included the Northern Harrier (Circus cyaneus) and Bobolink (Dolichonyx oryzivorus) in wet prairie, Bell’s Vireo (Vireo bellii) in early successional forest, and Northern Parula (Parula americana) and Prothonotary Warbler (Protonotaria citrea) in mature forest. Key Words: bird assemblage, early successional forest, floodplain forest, wet prairie

INTRODUCTION

in sand splays that made land unsuitable for agricultural production. This series of climatic events provided an opportunity for young forests and open prairie habitats to become established in the floodplain. Our study assessed bird distribution in these new habitats. Approximately half of the avian species breeding in the midwestern United States have declined significantly in the last several decades (Thompson et al. 1993). These declines are attributed in part to the degradation and loss of migration and breeding habitat. The lower Missouri River was once marked by frequent flooding, a shifting, braided channel, and high turbidity, resulting in a dynamic mosaic of wet prairie, early successional forest, and mature

Floodplain forests provide some of the most densely populated and diverse avian habitat in North America (Best et al. 1996). A number of studies have reported high species richness and high abundances of birds in these habitats (Best et al. 1996, Knutson et al. 1996, Twedt and Portwood 1997, Knutson and Klaas 1998, Twedt et al. 1999). Unfortunately, large floodplain forests in the midwestern United States are now facing a number of ecological challenges such as conversion to agriculture and urbanization. The lower Missouri River floodplain experienced severe and recurrent flood conditions in the 1990s (Chapman et al. 2004). As a result, large tracts of agricultural land were covered 552

Thogmartin et al., MISSOURI RIVER FLOODPLAIN BIRDS forest that was particularly suited to sustaining a diverse assemblage of birds. In the past century, major modifications to the river have occurred for flood protection, navigation, irrigation, and power production. The result is that the lower one-third of the Missouri River is channelized, leveed, and its banks are stabilized, reducing the scouring of mature habitat and the formation of sandbars upon which new habitat is created. Despite past anthropogenic modifications, the flood years of the early 1990s led to a reduction in agricultural production in the floodplain, presenting an opportunity for federal and state land management agencies to acquire new lands to add to the conservation estate (U.S. Army Corps of Engineers 2004). Initially, many acquisitions resulting from the 1990s floods were site specific and few included explicit ecological objectives. Acquisitions now include specific migratory and breeding bird objectives. Squaw Creek National Wildlife Refuge and Swan Lake National Wildlife Refuge were specifically established in the 1930s to provide migrating and breeding bird habitat. Efforts to understand contributions of these conservation areas for breeding and migratory birds are imperative for conserving species of special concern. Understanding the relationships between the floodplain avifauna and natural land cover of the lower Missouri River should benefit conservation efforts for birds. Our objective was to describe the spring migrating and summer breeding bird assemblage associated with three stages of forest succession in the lower Missouri River floodplain: open areas dominated by wet prairie/forbs, early successional forests, and mature forests. While latitudinal gradients in avian species diversity are well known (Pianka 1966, Tramer 1974), biogeographical gradients along a longitudinal axis are less commonly considered. We tested the hypothesis that avian species diversity and composition would vary along the east-west gradient associated with the lower Missouri River, ostensibly as a function of an east-west gradient in primary productivity. We anticipated that the greatest variation in community composition would occur among habitats, with minimal annual variation. Lastly, we identified species indicative of each habitat that might serve as sentinels of community integrity (Dufreńe and Legendre 1997). METHODS Ten study sites were chosen within the lower Missouri River alluvial floodplain, stretching from northwestern Missouri (near St. Joseph) to eastcentral Missouri (near St. Louis) (Table 1, Fig-

553

ure 1). These 10 sites were located in three United States Fish and Wildlife Service National Wildlife Refuges (Big Muddy, Swan Lake, and Squaw Creek), three Missouri Department of Conservation Areas (Overton Bottoms South, Eagle Bluffs, and Howell Island), and the Department of Defense’s Fort Leavenworth. All sites were on public land and all except two (Swan Lake and Squaw Creek) were riverward of a levee. The study region is characterized by loess deposits ranging from 3 to 27 m deep, overlaying limestone bedrock and bounded by limestone and sandstone bluffs (U.S. Fish and Wildlife Service 1999). Soils are generally moderately well drained to well drained, consisting of Haynie and Waldron Soil Series soils (U.S. Fish and Wildlife Service 1999). The western areas are characterized by a mix of clay, sand, gravel, and boulders deposited by glacial action and dissected by glacial runoff, and the eastern areas by a broad plateau dissected by erosion. The river floodplain varies in width from 3 to 16 km, with low river benches, terraces, and the remains of former river channels being common (U.S. Fish and Wildlife Service 1999). Land cover at the various study sites consisted of wet prairie, early successional forest, and mature forest. Floodplain wet prairie, possessing , 5% tree coverage, was comprised of horseweed (Conyza), aster (Symphyotrichum), goldenrod (Solidago), smartweed (Polygonum), pigweed (Amaranthus), bulrushes (Scirpu), cattail (Typha), prairie cordgrass (Spartina), sedges (Carex, Cyperus, Eleocharis), rice cutgrass (Leersia), reed canarygrass (Phalaris arundinacea), and millet (Echinochloa) (Nelson 1987, Young et al. 2004). Early successional forest was comprised of densely forested habitat with trees , 10 years of age. Dominant tree species were eastern cottonwood (Populus deltoides), willows (Salix), box elder (Acer negundo), ash (Fraxinus), dogwood (Cornus), and mulberry (Morus). Mature forest consisted of upper canopy trees . 15 m tall with dominant species of eastern cottonwood, box elder, pin oak (Quercus palustris), swamp white oak (Q. bicolor), silver maple (A. saccharinum), slippery elm (Ulmus rubra), hackberry (Celtis occidentalis), mulberry, and willow. The understory of mature forest was typically open, with few shrubs and midstory trees (Young et al. 2004). Until the floods of 1993 much of the habitat now in early successional forest and wet prairie was in active row crop agriculture. Prior to farming, habitat was either forest that was cut, burned, and stumped or stabilized floodplain created from the accumulation of sediment behind navigational wing dikes.

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WETLANDS, Volume 29, No. 2, 2009

Table 1. Mean (standard deviation) number of observed species per point count location and indices of diversity for 10 sites between 2002–2004, ordered from west to east along the lower Missouri River. S is species richness, H9 is ShannonWiener diversity, E is Shannon-Wiener species evenness, and D9 is Simpson’s diversity index. The mean across sites is an unweighted mean (and standard deviation). Site and acronym

Mean

SD

S

H9

E

D9

Squaw Creek, SQC Fort Leavenworth, FTL Swan Lake, SWL Lisbon Island, LIS Jameson Island, JAM Overton Bottoms North, OVN Overton Bottoms South, OVS Eagle Bluff, EBL St. Aubert’s Island, STA Howell Island, HOW Grand Mean

26.8 11.0 12.2 10.1 15.0 8.9 18.9 8.1 7.5 11.8 13.0

68.9 24.9 24.3 23.7 34.5 21.4 39.9 15.7 16.1 22.8 29.2

130 70 99 85 92 100 125 101 77 111 99 (19)

3.73 3.61 3.88 3.65 3.68 3.70 3.88 3.92 3.71 3.94 3.77 (0.12)

0.78 0.85 0.84 0.82 0.81 0.80 0.80 0.85 0.85 0.84 0.82 (0.03)

0.96 0.97 0.97 0.96 0.97 0.96 0.97 0.97 0.97 0.97 0.97 (0.01)

Bird data were collected each year in spring (15 April–14 May) and summer (15 May–30 June) in 2002–2004 at up to 365 locations (survey points), spaced $ 250 m apart. Counts were conducted within a half hour before sunrise to approximately three hours after sunrise. Migration occurred during spring, and breeding during summer. Survey points were a stratified random sample from the three habitat types at the 10 study areas. Each point was off-road and at least 100 m inside the habitat edge. Habitat types were defined based on digital maps of the study areas, aerial photos, and field reconnaissance (Young et al. 2004). All bird surveys were conducted using 5-min point counts within a 50-m radius circle (7,854 m2; Ralph et al. 1993). There were nine observers over the course of the survey. The number of points surveyed varied yearly, depending on weather conditions and other logistical limitations. We summarized species assemblages with study area-specific measures of species richness (S), Shannon-Wiener diversity (H9), Shannon-Wiener species evenness (E), and Simpson’s diversity index (D9; Magurran 2003). Species richness is the number of species in an assemblage. The Shannon-Wiener diversity accounts for both richness and relative S P abundance and is defined by: H 0 ~{ pi ln pi , i~1

where S is richness, pi is the proportion of individuals found in the ith species, and ln is the natural logarithm. Values generally range from 1.5 to 3.5, with H9 increasing as both a greater number of species and a more even distribution of species is measured. Shannon-Wiener species evenness is the actual diversity compared to the maximum possible diversity, defined by E 5 H9/ln[S], and constrained between 0 and 1. When there are similar proportions of all species, evenness is near one, whereas when

abundances are dissimilar (i.e., some rare and some common species), the value approaches zero. Simpson’s Index is considered a dominance index because it weights towards the abundance of the more common species, and provides the probability of any two individuals drawn at random from an infinitely large community belonging to different species. The bias corrected form of Simpson’s Index S P ðni ðni {1ÞÞ is: Ds ~ ðN ðN{1ÞÞ, where S in the richness, ni is the i~1

number of individuals in the ith species, and N is the total number of individuals of all species. We examined spatial patterning in study site measures of diversity by mapping and linearly regressing the diversity measures against latitude, longitude, and their interaction. We also controlled for species diversity increasing as a function of survey effort (i.e., the number of samples) by including the number of point counts as a covariate. We compared all possible combinations of the geographic coordinates and number of point counts against the responses with Akaike’s Information Criterion (AIC; Burnham and Anderson 2002) and selected the model with the lowest AIC. We focused our subsequent analysis on describing the bird assemblages associated with each habitat type. We tested for group differences in avian community composition among years, seasons, and study areas. To this end, we used non-metric multidimensional scaling (NMS) to assess whether the bird assemblages were different among these factor variables (McCune and Mefford 1999). NMS is a non-parametric approach appropriate for extremely skewed species data. The Bray-Curtis similarity metric was used to describe and ordinate similarities in bird community structure among sites (Legendre and Legendre 1998). The number of axes

Thogmartin et al., MISSOURI RIVER FLOODPLAIN BIRDS

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Figure 1. Study site locations along the lower Missouri River. See Table 1 for study area acronyms. ESF is early successional floodplain forest, MTF is mature forest, and WTP is wet prairie.

556 used in the ordination (two dimensional or three dimensional) was determined by stress level; stress is a measure of the distortion produced by compressing multi-dimensional data into a reduced set of dimensions and will increase as the number of axes (i.e., dimensions) is reduced. Low stress levels (i.e., , 0.1) indicate that the relative position of samples in ordinate space are a good reflection of the similarity of the avian community; high stress levels (i.e., . 0.25) indicate poor compression of the multidimensional data to a reduced set of dimensions (Clarke and Warwick 2001). Before ordination, the species matrix was transformed to presence/ absence to allow for the retention of 87 species that would have otherwise been deleted due to their rarity. One sample where only European Starlings (Sturnus vulgaris) were recorded and another sample where only two Savannah Sparrows (Passerculus sandwichensis) were recorded were deleted. We tested for variation in avian community composition among cover types, seasons, years, and study areas with the ANOSIM (Analysis of Similarities) procedure of PRIMER 5.2.9. Analysis of Similarities analyzes the similarities of groups relative to random groups in ordinate space based upon a permutation of the original groups, testing the null hypothesis that there were no assemblage differences among groups (Clarke and Gorley 2001). We used 999 permutations for each analysis of similarity. An RANOSIM statistic results from these permutations as a relative measure of separation among the groups. R-values can be categorized into three general groupings (Clarke and Gorley 2001): R . 0.75 indicated large difference among groups (clearly separable), R . 0.50 indicated clear differences, but the groups are overlapping, and R , 0.25 indicated minimal difference among groups (non-separable). It was not possible to test for study area (n 5 9) 3 cover type (n 5 3) 3 season (n 5 2) 3 year (n 5 3) interaction because partitioning the data into the total number of classes (n 5 162) yielded too few subjects to detect differences among groups (mean n < 11 subjects per group). Thus, we tested for univariate differences, except for the case of seasonal differences nested within years. We acknowledge that univariate assessment risked confounding effects of one factor (e.g., study area) with another (e.g., cover type). To explore the relative contributions of individual species to (dis)similarity among cover types we used SIMPER in PRIMER (Clarke 1993). Dissimilarity was measured with the Bray-Curtis dissimilarity index. The consistency of species in different cover types is indicated by the standard deviation of the

WETLANDS, Volume 29, No. 2, 2009 dissimiliarities. A large ratio of mean dissimilarity in species occurrence among cover types indicates that a species contributes substantially and consistently to dissimilarity in avian community composition among cover types. Indicator species analysis (Dufreńe and Legendre 1997) was used to sort the species by cover type and score their associations to those cover types (PCORD, McCune and Mefford 1999, McCune et al. 2002). This analysis provided a statistical basis for assigning a bird species to a primary cover type and defining a bird assemblage for each cover type. An indicator species is one most likely to be found in only one cover type, whereas similarity simply identifies those species most commonly found across sites within a cover type class (Dufreńe and Legendre 1997). Thus, species identified as commonly occurring in one cover type may not be indicative if it is also regularly found in another cover type. For the sake of brevity, we present only the species most indicative of each habitat; results for each species can be found in Thogmartin et al. (2005). RESULTS We recorded 131 species in wet prairie from 869 point count surveys during 2002–2004. Red-winged blackbird (Agelaius phoeniceus), Common Yellowthroat (Geothlypis trichas), and Dickcissel (a species of conservation concern) were the most ubiquitous species, each occurring at a frequency of . 50% and a mean count of . 2 birds/visit (Table 2, Figure 2). The majority of species (79%) were infrequently counted (mean count , 0.1 bird/visit). We recorded 121 species in early successional floodplain forest from 673 surveys during 2002– 2004. Indigo Bunting (Passerina cyanea), Northern Cardinal (Cardinalis cardinalis), and Common Yellowthroat were the most commonly occurring species in early successional forest, each occurring with a frequency of . 50% (Table 2). In addition to Indigo Bunting and Northern Cardinal, American Goldfinch (Carduelis tristis) was an abundant species, averaging . 1 bird/visit. Similar to wet prairie, the majority of species (72%) in early successional floodplain forest were infrequently counted. In mature forest, 141 species were recorded during 2002–2004. The most ubiquitous species were House Wren (Troglodytes aedon), Northern Cardinal, Indigo Bunting, and Red-bellied Woodpecker (Melanerpes carolinus), each occurring with a frequency of . 45% and a mean count of . 1 bird/visit. Most (69%) species were infrequently counted (Table 2). Species composition and diversity varied to some extent among study areas (Table 1). There was a


557

Table 2. Summarization of counts, ordered from most abundant to least abundant within habitat, for the most common species and species of conservation concern, as identified in surveys conducted in wet floodplain prairie (WTP), early successional forest (ESF), and mature forest (MTF) sites along the lower Missouri River between 2002–2004. The maximum observed was the maximum count in any single visit. Common Name Red-winged Blackbird Common Yellowthroat Dickcissel* Mallard# Orchard Oriole* Blue-winged Teal# Yellow-breasted Chat*# Eastern Meadowlark*# Field Sparrow* Bell’s Vireo*e Henslow’s Sparrow*# Grasshopper Sparrow* Greater Yellowlegs# Red-headed Woodpecker*# Eastern Wood-Pewee* American Bittern+ Rose-breasted Grosbeak* White-eyed Vireo* Great-Crested Flycatcher* Wood Thrush*# Least Bitterne Bald Eagle@ Indigo Bunting Northern Cardinal American Goldfinch Baltimore Oriole Common Yellowthroat Brown-headed Cowbird Yellow-billed Cuckoo American Crow Rose-breasted Grosbeak* Bell’s Vireo*e Cerulean Warbler*e Least Bitterne House Wren Northern Cardinal Indigo Bunting Red-bellied Woodpecker Rose-breasted Grosbeak* Cerulean Warbler*e Red-shouldered Hawke

Land Cover

Proportion Of Occurrence

Total Birds Counted

WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP ESF ESF ESF ESF ESF ESF ESF ESF ESF ESF ESF ESF MTF MTF MTF MTF MTF MTF MTF

0.937 0.745 0.566 0.084 0.086 0.044 0.059 0.052 0.043 0.030 0.025 0.024 0.008 0.015 0.012 0.012 0.009 0.009 0.007 0.002 0.001 0.001 0.842 0.605 0.367 0.495 0.507 0.416 0.467 0.370 0.183 0.088 0.003 0.001 0.485 0.622 0.495 0.681 0.333 0.034 0.023

7,494 1,766 1,749 193 129 109 69 64 61 42 32 30 24 14 13 13 11 9 6 3 1 1 2,108 716 715 637 636 607 551 510 216 103 2 1 1,166 1,035 1,017 921 569 30 26

Mean Count Standard Maximum Per Visit Deviation Per Visit Observed 8.624 2.032 2.013 0.222 0.148 0.125 0.079 0.074 0.070 0.048 0.037 0.035 0.028 0.016 0.015 0.015 0.013 0.010 0.007 0.003 0.001 0.001 3.132 1.064 1.062 0.947 0.945 0.902 0.819 0.758 0.321 0.153 0.003 0.001 1.350 1.198 1.177 1.066 0.659 0.035 0.030

15.007 1.780 2.400 1.063 0.572 1.149 0.365 0.371 0.419 0.315 0.256 0.238 0.482 0.135 0.147 0.155 0.147 0.112 0.083 0.076 0.034 0.034 2.460 1.276 2.056 1.389 1.383 1.495 1.096 1.213 1.098 0.571 0.054 0.039 1.839 1.416 1.561 1.045 1.379 0.189 0.213

238 9 16 20 5 30 4 5 6 4 3 3 13 2 2 3 3 2 1 2 1 1 15 12 20 12 14 12 8 6 20 5 1 1 10 12 11 10 17 2 3

e

Missouri State Watch list. Missouri State endangered. Federal Threatened Species. * Neotropical migratory landbird species of conservation concern and United States Fish and Wildlife Region 3 resource conservation priority. # Upper Mississippi River / Great Lakes Joint Venture focal species. +

@

longitudinal gradient in diversity, with each measure generally increasing from west to east (Table 3, Figure 2). St. Aubert’s Island had a species composition that overlapped that of Eagle Bluff, Jameson

Island, and Lisbon Bottoms, primarily because the species recorded at St. Aubert’s Island were fairly ubiquitous, the site was centrally located, and species richness was low. All other sites marginally

558


Figure 2. Plots of four avian species diversity measures (richness [S], Shannon-Wiener diversity [H9], ShannonWiener species evenness [E], and Simpson’s diversity index [D9]) as a partial function (dashed lines represent prediction intervals) of longitude from 10 locations along the lower Missouri River, 2002–2004. Note: west is on the left, east on the right.

differed from one another (Global RANOSIM 5 0.385, P 5 0.001). Avian communities among cover classes were distinguishable (Global RANOSIM 5 0.683, P 5 0.001; Figure 3). Mature forest tended to have a more diverse avian assemblage than wet prairie (Table 4). Although the numerical difference in avian richness was small, the greatest difference in avian species composition occurred between wet prairie and mature forest (RANOSIM 5 0.857; mean dissimilarity 5 92.2%). Early successional floodplain forest and wet prairie were also different (RANOSIM 5 0.721; mean dissimilarity 5 87.1%). There was no significant separation, however, between early successional and mature forests in their avifauna (RANOSIM 5 0.272; mean dissimilarity 5 75.1%). Early successional forest appeared to have an avian species composition intermediate to mature forest and wet prairie, coincident with the notion that the avian species community was responding to a gradient in succession. Avian community compositions overlapped considerably

among years and seasons (Global RANOSIM 5 0.611, P 5 0.133). Because we were able to dismiss annual differences in avian species composition, and there were marginal differences between seasons, we tested for a combined effect by calculating an analysis of similarities with season nested within cover class. Within land cover, avian species composition did not differ substantially between seasons (Global RANOSIM 5 0.236, P 5 0.001). Thus, variation in avian species composition could be largely attributed to cover class alone (Global RANOSIM 5 0.889, P 5 0.067). Nearly half of the avian species occurred in all three land cover types; 44.5% (n 5 77) and 53.2% (n 5 75) of species were found in the three land covers during the migration and breeding season, respectively, although some observations appeared to be incidental, such as Bell’s Vireo in mature forest. At least twice as many avian species were unique to wet prairie (n 5 33 and 28 during migration and breeding seasons, respectively) relative to species unique to either early successional forest (n 5 3 and 3) or mature forest (n 5 15 and 14). Some birds found in mature forest, but not early successional forest, were observed in wet prairie during migration (House Wren, Yellow-rumped Warbler [Dendroica coronata], Orange-crowned Warbler [Vermivora celata], Willow Flycatcher [Empidonax traillii], Wilson’s Warbler [Wilsonia pusilla], and Yellowthroated Warbler [Dendroica dominica]). The Killdeer (Charadrius vociferous), a wet prairie species, was observed in mature forest during migration. Species unique to wet prairie included American Bittern (Botaurus lentiginosus), American White Pelican (Pelecanus erythrorhynchos, only observed in migration), Grasshopper Sparrow (Ammodramus savannarum), Greater Yellowlegs (Tringa melanoleuca), Henslow’s Sparrow (A. henslowii), Horned Lark (Eremophila alpestris), Nelson’s Sharp-tailed Sparrow (A. nelsoni), Ring-necked Pheasant (Phasianus colchicus), and Sora (Porzana carolina). Eight percent of the avifauna occurring in wet prairie in the breeding season were not observed there during

Table 3. Best models describing avian species diversity as a consequence of geography along the lower Missouri River between 2002–2004. The model weight, or relative likelihood, for the best model relative to alternative models in each case was . 0.5. Diversity Measure Species Richness, S Shannon-Wiener Diversity, H9 Shannon-Wiener Evenness, E Simpson’s Diversity, D9

Best Model Longitude + Latitude + (Longitude 3 Latitude) + No. of Point Counts Longitude + Latitude Longitude + Latitude + (Longitude 3 Latitude) + No. of Point Counts Longitude

r2 0.69 0.47 0.74 0.42


559 DISCUSSION

Figure 3. Avian community compositional differences among cover classes, lower Missouri River, 2002–2004, based on a non-metric multidimensional scaling of taxonomic differences. Each bubble represents a single site in multidimensional space, with bubble size corresponding to the number of species observed at the site.

the migration period. Nearly a quarter of species observed in wet prairie were recorded only during the migration period. Only 2% of the early successional forest avifauna was unique to that habitat, with the Philadelphia Vireo being most notable. Fourteen species were unique to mature forest in both migration and breeding seasons, of which Barred Owl (Strix varia), Chimney Swift (Chaetura pelagica), and Red-shouldered Hawk (Buteo lineatus; in migration) were the most common. Yellow-rumped Warblers and Yellow-throated Warblers were observed in mature forest during the breeding season only. Twenty-four indicator species (i.e., species representative of a habitat and its associated avian assemblage) were identified (Table 5). Northern Harrier and Bobolink were completely indicative of wet prairie habitat (both indicator values 100%), Bell’s Vireo was indicative of early successional floodplain forest (indicator value 5 86%), and Northern Parula and Prothonotary Warbler were the most significant indicators of mature forest (indicator values 5 73% and 84%, respectively).

Approximately one in every seven bird species in North America occurs in habitat along the lower Missouri River. For the lower Missouri River floodplain, we found avian diversity generally varied as a function of cover type, with smaller variation explained by regional location and season. The greatest assemblage diversity occurred in the breeding season in mature forest in the eastern portion of the floodplain, while the least diverse bird community occurred during migration in wet prairie in the western portion of the floodplain. Assemblage descriptions can be confounded by species detectability (Boulivier et al. 1998), and for many species in this study, detectability varied among season and cover type (Thogmartin et al. 2005). However, factors to correct counts were not evident. Thus, our diversity metrics must be viewed with caution because rare or difficult to observe species may have been under-sampled. The Northern Parula and Prothonotary Warbler were species indicative of mature forest on the lower Missouri River, making them apt targets for the monitoring of conservation interventions (National Ecological Assessment Team 2006). The Northern Parula generally builds nests in hanging bunches of epiphytic growth, beard moss (Usnea lichen) or lace lichen (Ramalina reticulata) (Petit 1999); thus, nesting sites are most often in areas where these epiphytes grow. The abundance of snags in mature forest likely make the Prothonotary Warbler indicative for this forest type, as this bird generally nests in cavities of large trees (Petit 1999). Preferred nesting sites for the Prothonotary Warbler are river bottoms, sloughs, and swamps, usually within 5 m of standing water or in low-lying, easily flooded areas. However, Northern Parula and Prothonotary Warbler are not useful indicators of forested riverine habitat along the Mississippi River (Twedt et al. 1999, Knutson et al. 2005). The only species commonly indicative to both the Mississippi Alluvial Valley and the lower Missouri River in mature

Table 4. Mean and standard deviation of observed number of bird species and indices of diversity for 3 cover types (wet floodplain prairie, WTP; early successional floodplain forest, ESF; and mature forest, MTF) along the lower Missouri River, 2002–2004. S is species richness, H9 is Shannon-Wiener diversity, E is Shannon-Wiener species evenness (H9/ln[S]), and D9 is Simpson’s diversity index. The grand mean is the mean in richness and diversity across all lower Missouri River locations, irrespective of cover type. Site

Mean

SD

S

H9

E

D9

WTP ESF MTF Grand Mean

28.7 34.9 67.3 43.6

91.9 78.0 124.5 98.1

131 127 139 132.3

3.497 3.799 3.978 3.758

0.717 0.784 0.806 0.769

0.937 0.967 0.975 0.960

560


Table 5. Indicator species sorted by cover type (wet prairie, WTP; early successional floodplain forest, ESF; and mature forest, MTF) and significance level for birds surveyed at 10 study locations along the lower Missouri River between 2002– 2004. The randomized mean and standard deviation are from 1,000 Monte Carlo permutations of the data; the observed indicator value represents the degree of concordance with the indicator cover type and is assessed relative to the randomized mean. Only those species with randomized p-values , 0.1 are included. Species Northern Harrier Bobolink Mallard European Starling Tree Swallow Nelson’s Sharp-tailed Sparrow Red-winged Blackbird Dickcissel Wood Duck Killdeer Northern Rough-winged Swallow Broad-winged Hawk Savannah Sparrow Eastern Kingbird Eastern Meadowlark Barn Swallow Red-tailed Hawk Chipping Sparrow Bell’s Vireo Prothonotary Warbler Acadian Flycatcher Northern Parula Chestnut-sided Warbler Summer Tanager

Cover Type

Observed Indicator Value (%)

Randomized Mean (%)

SD

p

WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP WTP ESF MTF MTF MTF MTF MTF

100.0 100.0 94.6 89.9 89.0 85.7 85.5 82.8 81.4 78.2 76.9 76.9 76.0 74.0 73.4 72.6 72.3 67.8 86.1 84.0 81.1 73.3 63.4 51.3

30.5 31.0 56.9 57.1 64.4 34.5 64.9 43.1 51.4 47.5 34.6 35.4 38.6 51.4 44.5 43.1 46.9 36.2 44.1 47.3 56.2 44.5 44.2 43.3

15.6 15.8 19.6 19 15.8 17.3 14.4 18.6 17.6 18.6 15.9 17.1 17.7 14.1 17.4 16.7 11.4 17.5 16.7 11.4 15.3 8.4 11.3 5.9

0.015 0.015 0.054 0.075 0.013 0.028 0.080 0.037 0.087 0.057 0.034 0.054 0.048 0.057 0.069 0.069 0.011 0.089 0.013 0.003 0.062 0.001 0.061 0.076

forest (bottomland hardwood forest in Twedt et al. 1999) was the Acadian Flycatcher. These biogeographic differences in indicator species among the lower Missouri River, middle Mississippi River, and Mississippi Alluvial Valley likely represent the accumulation of species range limits as one moves west to east (and to a lesser extent from south to north) (Tramer 1974 [Figure 3], Bock 1984). There was considerable overlap in species composition between early successional forest and the other two cover classes. Thus, only one indicator species, the Bell’s Vireo, was identified for early successional forest. This species occurs in dense, low, shrubby vegetation, brushy fields, and young second-growth forest or woodland (Brown 1993). Despite its indicator status, the Bell’s Vireo was uncommon in early successional forest, as it was only the 31st most frequently observed species in this cover type. Because of its rarity, it would be difficult to use this species for the monitoring of management activities in early successional forest on publicly managed lands unless the intensity of survey effort was great (Thogmartin et al. 2007).

The 100% indicator value of Northern Harrier and Bobolink for wet prairie makes them particularly useful targets for monitoring of conservation actions. The bird species assemblages that we found associated with wet prairie are typical for grasslands in central Missouri (Skinner et al. 1984, McCoy et al. 1999, Winter and Faaborg 1999) and eastern Kansas (near Fort Leavenworth; Zimmerman and Tatschel 1975). Red-winged Blackbirds were the most common species in wet prairie and were the only species indicative to both wet prairie in the lower Missouri River and shrub/scrub of the middle Mississippi River (Knutson et al. 2005). Because Red-winged Blackbirds can be a pest in agricultural ecosystems (Linz et al. 1993), farmers operating near wet prairie habitat on the lower Missouri River may negatively perceive conservation devoted to prairies. Even though wet prairie along the lower Missouri River provides habitat to relatively fewer species, this habitat remains important for the conservation of numerous species of concern (Table 2). Twenty species of some conservation concern were observed in wet prairie habitat, more than early and mature

Thogmartin et al., MISSOURI RIVER FLOODPLAIN BIRDS forest together, including Dickcissel, Orchard Oriole (Icterus spurius), Yellow-breasted Chat (Icteria virens), Eastern Meadowlark (Sturnella magna), Field Sparrow (Spizella pusilla), Bell’s Vireo, Henslow’s Sparrow, and Grasshopper Sparrow (see Thogmartin et al. 2005). While Dickcissel populations have declined since the mid-1960s (Sauer et al. 2005) and are ranked third in conservation concern for grassland birds in the midwestern United States by Herkert et al. (1996), Dickcissels were the third most observed wet prairie species. Despite considerable overlap among habitats in the bird species they share, maintaining an array of habitat conditions will conserve a complete avifauna. Wet prairie is largely an ephemeral habitat, and without natural processes associated with recurrent flooding, this habitat may need to be maintained by herbicide and mechanical treatments or prescribed fire. Allowing succession of these wet prairies to forest conditions could lead to a loss of the 20% of the avifauna unique to wet prairie habitat, including species of conservation concern. Approximately 17,000 ha of habitat were added to the conservation estate along the lower Missouri River as result of the abandonment of agricultural lands after the flooding of the 1990s. Thogmartin et al. (2005, 2009) identified geomorphological characteristics useful in differentiating the successional fate of these abandoned agricultural lands. They were able to successfully predict whether a site would succeed to wet prairie or to forest. With the assemblage information we provided, the relative role of these land acquisitions for their conservation value can now be assessed. Such evidence-based conservation is essential to the efficient allocation of scarce conservation resources (Pullin and Knight 2003, Sutherland et al. 2004, National Ecological Assessment Team 2006). ACKNOWLEDGMENTS Carl Korschgen, Shawn Papon, and Nick Bezzerides were partially responsible for project design and execution. Funding for this research was provided by the US Army Corp of Engineers, Kansas City District (with special thanks to Kelly Ryan and Glenn Covington), U.S. Fish and Wildlife Service Non-game bird program (with special thanks to Steve Lewis), USFWS Service Challenge Grant program (with special thanks to Steve Kufrin), Upper Mississippi River/Great Lakes Joint Venture (with special thanks to Barbara Pardo), and Missouri Department of Conservation (with special thanks to Kent Korthas, Tim James, and John Vogel). Technical assistance was provided by Sara

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Acosta, Tim Altnether, Shawn Cooksey, Sean Counihan, Andrea Estes, Jack Finley, Justin Friedrich, Amanda Griffin, Heather Lambert-Dougherty, Jessica Lee, Shawn Papon, Tommie Rogers, and Pete Sullivan. Molly Comstock provided project logistics. This manuscript was substantially improved by comments from Wedge Watkins and anonymous reviewers. LITERATURE CITED Best, L. B., K. E. Freemark, B. S. Steiner, and T. M. Bergin. 1996. Life history and status classifications of birds breeding in Iowa. Journal of the Iowa Academy of Science 103:34–45. Boulinier, T., J. D. Nichols, J. R. Sauer, J. E. Hines, and K. H. Pollock. 1998. Estimating species richness to make inference in community ecology: the importance of heterogeneity in species detectability as shown from capture-recapture analyses of North American Breeding Bird Survey Data. Ecology 79:1018–28. Brown, B. T. 1993. Bell’s Vireo. In A. Poole, P. Stettenheim, and F. Gill (eds.) The Birds of North America, No. 35. The Academy of Natural Sciences, Philadelphia, PA, USA. Burnham, K. P. and D. R. Anderson. 2002. Model Selection and Multimodel Inference: a Practical Information-Theoretic Approach. Second edition. Springer-Verlag, New York, NY, USA. Chapman, D. C., E. A. Ehrhardt, J. F. Fairchild, R. B. Jacobson, B. C. Poulton, L. C. Sappington, B. P. Kelly, and W. R. Mabee. 2004. Ecological dynamics of wetlands at Lisbon Bottom, Big Muddy National Fish and Wildlife Refuge, Missouri. U.S. Geological Survey, Open File Report 20041036. Clarke, K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18:117–43. Clarke, K. R. and R. N. Gorley. 2001. PRIMER v5: Users Manual/Tutorial. PRIMER-E Ltd, Plymouth, UK. Clarke, K. R. and R. M. Warwick. 2001. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation, Second edition. PRIMER-E Ltd, Plymouth, UK. Dufreńe, M. and P. Legendre. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monograph 67:345–66. Herkert, J. R., D. W. Sample, and R. E. Warner. 1996. Management of midwestern grassland landscapes for the conservation of migratory birds. p. 89–116. In F. R. Thompson III (ed.) Management of Midwestern Landscapes for the Conservation of Neotropical Migratory Birds. USDA Forest Service Gen. Tech. Rep. NC-187. USDA Forest Service North Central Forest Experiment Station, St. Paul, MN, USA. Knutson, M. G., J. P. Hoover, and E. E. Klaas. 1996. The importance of floodplain forests in the conservation and management of neotropical migratory birds in the Midwest. p. 168–88. In F. R. Thompson III (ed.) Management of Midwestern Landscapes for the Conservation of Neotropical Migratory Birds. General Technical Report NC-187. U.S. Forest Service, North Central Forest Experiment Station, St. Paul, MN, USA. Knutson, M. G. and E. E. Klaas. 1998. Floodplain forest loss and changes in forest community composition and structure in the Upper Mississippi River: a wildlife habitat at risk. Natural Areas Journal 18:138–50. Knutson, M. G., L. E. McColl, and S. A. Timm. 2005. Breeding bird assemblages associated with stages of forest succession in large river floodplains. Natural Areas Journal 25:55–70. Legendre, P. and L. Legendre. 1998. Numerical Ecology. Second English edition. Elsevier Science BV, Amsterdam, Netherlands.

562 Linz, G. M., R. A. Dolbeer, J. J. Hanzel, and L. E. Huffman. 1993. Controlling blackbird damage to sunflower and grain crops in the Northern Great Plains. U.S. Department of Agriculture, Agriculture Information Bulletin 679, Washington, DC, USA. Magurran, A. E. 2003. Ecological Diversity and its Measurement. Princeton University Press, Princeton, NJ, USA. McCoy, T. D., M. R. Ryan, E. W. Kurzejeski, and L. W. Burger, Jr. 1999. Conservation reserve program: source or sink habitat for grassland birds in Missouri? Journal of Wildlife Management 63:530–38. McCune, B. and M. J. Mefford. 1999. PC-ORD. Multivariate Analysis of Ecological Data. Version 4.0 for Windows. MjM Software Design, Gleneden Beach, OR, USA. McCune, B., J. B. Grace, and D. L. McCune. 2002. Analysis of Ecological Communities. MjM Software Design, Gleneden Beach, OR, USA. National Ecological Assessment Team. 2006. Strategic Habitat Conservation handbook: a report from the National Ecological Assessent Team – 29 June 2006. U.S. Fish and Wildlife Service, Arlington, VA, USA, and U.S. Geological Survey, Reston, VA, USA. Petit, L. J. 1999. Prothonotary Warbler (Protonotaria citrea). In A. Poole and F. Gill (eds.) The Birds of North America, No. 408. The Birds of North America, Inc., Philadelphia, PA, USA. Pianka, E. R. 1966. Latitudinal gradients in species diversity: a review of concepts. American Naturalist 100:33–46. Pullin, A. S. and T. M. Knight. 2003. Support for decision making in conservation practice: an evidence-based approach. Journal of Nature Conservation 11:83–90. Ralph, C. J., G. R. Geupel, P. Pyle, T. E. Martin, and D. F. DeSante. 1993. Handbook of Field Methods for Monitoring Landbirds. United States Department of Agriculture General Technical Report PSW-GTR-144. Sauer, J. R., J. E. Hines, and J. Fallon. 2005. The North American Breeding Bird Survey, Results and Analysis 1966– 2004. Version 2005.2. United States Geological Survey Patuxent Wildlife Research Center, Laurel, MD, USA. URL: ,http://www.mbr-pwrc.usgs.gov/cgi-bin/atlasa99.pl?06040&1&04. (accessed 3 June 2005). Skinner, R. M., T. S. Baskett, and M. D. Blenden. 1984. Bird habitat on Missouri prairies. Terrestrial Series #14. Missouri Department of Conservation, Jefferson City, MO, USA. Sutherland, W. J., A. S. Pullin, P. M. Dolman, and T. M. Knight. 2004. The need for evidence-based conservation. Trends in Ecology and Evolution 19:305–08.

WETLANDS, Volume 29, No. 2, 2009 Thogmartin, W. E., M. Gallagher, N. Young, J. J. Rohweder, and M. G. Knutson. 2009. Factors associated with succession of abandoned agricultural lands along the lower Missouri River. Restoration Ecology, 17:290–96. Thogmartin, W. E., B. R. Gray, M. Gallagher, N. Young, J. J. Rohweder, and M. G. Knutson. 2007. Power to detect trend in short-term time series of bird abundance. Condor 109:943–948. Thogmartin, W. E., M. G. Knutson, J. J. Rohweder, and B. R. Gray. 2005. Bird habitat associations in the lower Missouri River floodplain: a final report to the U.S. Fish and Wildlife Service Big Muddy National Wildlife and Fish Refuge. United States Geological Survey Upper Midwest Environmental Sciences Center, La Crosse, WI, USA. Thompson III, F. R., S. J. Lewis, J. Green, and D. Ewert. 1993. Status of Neotropical migrant landbirds in the Midwest: Identifying species of management concern. p. 145–158. In D. M. Finch and P. W. Stangel (eds.) Status and Management of Neotropical Migratory Birds. U.S. Department of Agriculture, Forest Service General Technical Report RM-229. Tramer, E. J. 1974. On latitudinal gradients in avian diversity. Condor 76:123–30. Twedt, D. J. and J. Portwood. 1997. Bottomland hardwood reforestation for neotropical migratory birds: are we missing the forest for the trees? Wildlife Society Bulletin 25:647–52. Twedt, D. J., R. R. Wilson, J. L. Henne-Kerr, and R. B. Hamilton. 1999. Impact of forest type and management strategy on avian densities in the Mississippi Alluvial Valley, USA. Forest Ecology and Management 123:261–74. U.S. Army Corps of Engineers. Missouri River bank stabilization and navigation project, fish and wildlife mitigation project, annual implementation report. United States Army Corps of Engineers, Omaha District, Omaha, Nebraska, and Kansas City District, Kansas City, MO, USA. URL: ,http://www. nwd.usace.army.mil. (accessed Sept. 13, 2005). U.S. Fish and Wildlife Service. 1999. Big Muddy National Fish and Wildlife Refuge Final Environmental Impacts Statement, Puxico, MO, USA. Winter, M. and J. Faaborg. 1999. Patterns of area sensitivity in grassland-nesting birds. Conservation Biology 13:1424–36. Young, N. B., M. A. Gallagher, and S. G. Papon. 2004. Distribution and abundance of migrant and breeding songbirds in floodplain habitats of the lower Missouri River watershed – 2003 Annual Report. U.S. Fish and Wildlife Service Big Muddy National Fish and Wildlife Refuge, Columbia, MO, USA. Zimmerman, J. L. and J. L. Tatschel. 1975. Floodplain birds of Weston Bend, Missouri River. Wilson Bulletin 87:196–206. Manuscript received 12 March 2008; accepted 13 November 2008.