Assessing migration patterns in Passerina ciris using the world’s bird collections as an aggregated resource

Focal taxon

The Painted Bunting (Passerina ciris) is a migratory New World passerine in the family Cardinalidae. Current taxonomy recognizes two subspecies of Painted Bunting but the boundary between these races does not coincide with a nearly 500 km gap separating the east coast and the Midwestern breeding populations of Painted Buntings (Thompson, 1991). Further, these isolated breeding populations differ dramatically in their molt scheduling, with the eastern population molting on its breeding range prior to migration and the Midwestern population moving to the monsoon region of the southwestern United States and northwestern Mexico where it pauses to molt before proceeding to its wintering range in southern Mexico and Central America (Thompson, 1991; Rohwer, Butler & Froehlich, 2005; Rohwer, Rohwer & Ramírez, 2009). In this study, we focus exclusively on the Midwestern breeding population of Painted Bunting.

Across their range, Painted Buntings favor ecotones with brushy, weedy habitats in second growth, and dense forest understory. Relatively little is known about the species’ movements following molt stopover, but progressive southward movements of populations along the west coast of Mexico have been observed in the autumn (S Rohwer, pers. comm., 2014; Contina et al., 2013).

Calculating abundance indices

To track spatial and temporal changes in Painted Bunting population densities during the wintering season, we employed a method of inferring relative population densities from specimen collections data known as Abundance Indices. The method, proposed in Rohwer et al. (2012) and developed independently by Miki et al. (2000), adjusts for a major shortcoming of specimen collections data—the absence of associated information on collecting effort—by producing an index that is corrected to a crude measure of effort. To produce an abundance index, electronic natural history museum catalogs (such as VertNet.org) are used to aggregate NHC specimen records of (1) the species of interest and (2) other taxa that are typically collected with similar methods to the species of interest. Raw counts are then used to determine the proportion of focal species specimens to all collected specimens from a particular region and time period, allowing for comparisons of abundance across regions with different histories of collecting effort.

We used the formula for abundance index calculation proposed in Rohwer, Grason & Navarro-Siguenza (2015): ${\displaystyle A{I}_{kr}=100\frac{{\chi }_{kr}}{\sum _{j=1}^n{\chi }_{jr}}}$ where χ_kr is number of specimens of the kth species collected in r, the region and time period of interest, and n is the number of specimens of all species that would be “expected” to be collected using the same methods in that region and time period of interest.

Reference data

In order to calculate abundance indices for Painted Buntings, we accessed two databases of specimen collection records: the Mexican Bird Atlas, and VertNet. The Mexican Bird Atlas began compilation by A. Navarro and T. Peterson in the 1990s, and now represents the most complete reference of study skins of Mexican birds residing in natural history museums worldwide (Navarro-Siguenza, Peterson & Gordillo-Martínez, 2003). The Atlas now contains records of more than 370,000 specimens from 71 museums, and is completely georeferenced (meaning each specimen record is associated with the latitude and longitude of its collection locality). We used records for the Mexican Bird atlas for all indices calculated within the political boundaries of Mexico. The VertNet data portal (VertNet.org) is an NSF-funded collaborative project to make biodiversity information, including specimen collections records, freely and easily accessible to the public. We used records from VertNet to examine raw bunting counts by month for the Central American countries of Guatemala, El Salvador, Honduras, Nicaragua, Costa Rica, and Panama.

Subsetting and data cleaning

We produced abundance indices for Painted Buntings for each month of the year. These indices were produced on a relatively fine spatial scale for Mexico (a 5 min latitude by 5 min longitude grid), but were only produced on a country-wide level for Central America, due to the limited number of properly georeferenced records in the VertNet data. To calculate abundance indices, we referenced Painted Bunting collections against the combined records of species collected using similar methods. We follow Rohwer et al. (2012) in including other taxa commonly collected with mist-nets and small-bore shotguns: Passerines (order Passeriformes), Cuckoos (order Cuculiformes), and Woodpeckers (order Piciformes; family Picidae). While abundance index values are sensitive to reference specimen selection and collection bias (e.g., collectors disproportionately targeting rare species), we believe the high species diversity and large number (>245,000) of specimens included in our reference specimen database minimize the influence of this shortcoming on our conclusions.

Despite the fact that majority of specimen collections records accessed from the Mexican Bird Atlas were both dated and georeferenced, a subset (<10% in both Painted Bunting and reference specimen data) had either missing or obviously erroneous values for date or latitude and longitude coordinates. These were excluded from all subsequent analyses.

Analyzing migration patterns

We used a Geographic Information Systems (GIS) approach to plot all specimen collections records from the Mexican Bird Atlas, for both Painted Buntings and reference specimens. A 5-minute raster grid was initially overlayed on plotted reference specimens, which were then transformed into a scaled map of all collected specimens in a particular region and month. In any grid square where Painted Bunting specimens were collected, an abundance index was calculated and plotted as a circle, its diameter proportional to the value of the index. Although abundance indices were produced for Central America, we did not incorporate these into our geospatial analysis due to exceedingly few Painted Bunting specimens and corresponding low AI values.

To determine the statistical significance of any observed patterns of spatial and temporal change, we divided Mexico into three regions corresponding with contiguous bands of Painted Bunting habitat, (NW, NE, and S, defined by the 20th parallel north and the 103rd meridian West, respectively; Fig. 1). Among these regions, we performed three Pearson’s chi-square tests for changes in abundance indices in Painted Buntings and reference specimens during three time periods: the molt-stopover period (July–October), winter (November–February), and spring migration (March and April). Specifically, we asked (1) whether Painted Bunting records were significantly more numerous than expected by chance (relative to reference specimens) in NW Mexico than NE Mexico during the molting season; (2) whether Painted Bunting records were significantly more numerous than expected by chance in Southern Mexico than NW Mexico during the winter; and (3) whether Painted Bunting records were significantly more numerous than expected by chance in NE Mexico (along the Gulf of Mexico) than in NW Mexico during spring migration. To account for the possibility that migrants from the Southeastern US population of Painted Buntings were wintering on the Yucatán Peninsula and thus inflating specimen densities to the extent that they influenced statistical significance of our results, we repeated our comparison of records in Southern Mexico and NW Mexico excluding all records east of the Isthmus of Tehuantepec (at 94°West). Additionally, to evaluate a hypothesis based on observations by S Rohwer (pers. comm., 2015) that Painted Buntings were primarily restricted to coastal lowlands during the non-breeding season, we performed a chi-square test to determine whether Painted Bunting records were significantly more numerous below 200 m in elevation. We display contingency tables for these tests and our predictions for relative specimen densities consistent with a pattern of circular movement around coastal Mexico in Fig. 1. This aggregated measure of abundance change allowed us to rigorously test our interpretation of the direction of migration.

Finally, to provide additional ecological context to our findings, we investigated the correlation between bunting abundance and primary productivity. We downloaded monthly means for the Enhanced Vegetation Index (EVI) compiled from 2000 to 2010 from the North American Vegetation Index and Phenology Lab website (http://vip.arizona.edu). We used EVI, as opposed to the more widely used Normalized Difference Vegetation Index (NDVI), as an index of primary productivity because of EVI’s enhanced sensitivity in high biomass regions (such as the Painted Buntings’ wintering sites) and its robustness against atmospheric influences (Liu & Huete, 1995; Matsushita et al., 2007). The downloaded data for each monthly mean consisted of a georeferenced HDF raster file at a 0.05°resolution. We extracted the EVI data layer and clipped it to the area of interest (Latitude: 10 to 40°, Longitude: −125 to −70°).

For each month, we extracted EVI values for pixels within a 10 km radius of each collection site. We included data from each specimen such that locations from which multiple specimens were collected were represented multiple times in the data set. We assume that collection sites that yielded multiple birds are indicative of the most suitable or desirable habitat for Painted Buntings, and that they should be weighted in a corresponding manner when evaluating the relationship between EVI and Painted Bunting distributions.

To test the simple null hypothesis that specimen locations for Painted Buntings were random with respect to EVI, we generated 500 uniformly random locations within the borders of Mexico and repeated the extraction process described above with each monthly EVI map and the 500 random points. We averaged the pixels from each location and then compared the set of EVI values for each month from the specimen locations to the corresponding EVI values associated with the random locations. We performed a t-test for each monthly data set and calculated 95% confidence intervals for each overall mean.

Because randomly chosen points are not necessarily a good representation of available habitat for Painted Buntings, and because of non-independence of some Painted Bunting collecting sites (those that are repeated in the analysis) we generated what is arguably a more comparable set of reference locations by randomly choosing 250 locations for each month from the museum reference data described above. This subsampling process began by rounding the coordinates (latitude and longitude) of all locations to the nearest 0.01°(about 1 km). We then sampled 250 unique locations from the specimen data, and we dervied EVI values for each location as described above. We filtered out locations where there were fewer than three resulting EVI pixels within the buffer area (such low pixel counts can result from sites surrounded by null pixels associated with water bodies). We then duplicated each EVI score according to how many times it was represented in the entire data set for the relevant month. These subsamples allowed us to effectively weight each location based on the total number of birds collected there in a manner similar to the weighting of the Painted Bunting collection that resulted from repeated location data.

Initial manipulation of EVI data was performed using the gdal translator library (http://www.gdal.org). All subsequent analysis were performed in R version 3.1.0 (R Core Team, 2014) using the following packages: raster (Bivand & Rundel, 2015), maptools (Bivand & Lewin-Koh, 2015), plyr (Wickham, 2011), rgeos (Bivand & Rundel, 2015), and ggplot2 (Wickham, 2009).

Migration analysis

Our plotted monthly abundance indices for P. ciris confirm a pattern of population-level movement across Mexico throughout the year (Fig. 2 and Table 1). AI values plotted for July illustrate an east–west split during mid-summer, with high AI values forming two clusters in Northern Mexico: an eastern cluster in Nuevo Leon and Tamalpais, and a western cluster in Sinaloa and Durango. In August and September, these associations persist, with the western cluster increasing both by number of raster grid squares reporting an abundance index, and by value of plotted abundance indices. October, November, and December show the southward movement and diffusion of plotted AI values on both coasts of Mexico. Abundance indices again hug the states of both coasts, forming a loose western cluster in Guerrero, Michoacán, Oaxaca, Jalisco, and Colima, and a loose eastern cluster in the Veracruz, Tabasco, Campeche, and Yucatån. Although there is then no observable pattern in plotted AI values from January to February within or among these clusters, this period is followed by a strong association of AI values in northeast Mexico (Coahuila, Nuevo Leon, Tamalpais) and an absence of values elsewhere in the months of March and April. South of Mexico, specimen records indicate the presence of Painted Buntings at extremely low densities, mostly restricted to the winter months of November to March. Pooled raw counts of buntings for all records in this region (including Belize, El Salvador, Honduras, Guatemala, Nicaragua, Costa Rica, and Panama) confirm the near absence (n < 10 per month) of bunting specimens collected during the July–October stopover period (Fig. 3).

Statistical tests

Our chi-sq tests confirm significantly higher Painted Bunting record abundance than expected for all four analyses. Painted Buntings were (1) significantly more numerous in NW Mexico than NE Mexico during the molt-stopover period compared to reference specimens (question 1; X-squared = 108.8812, df = 1, p-value < 0.0005), (2) significantly more numerous in southern than NW Mexico in the winter than reference specimens (question 2; X-squared = 46.6711, df = 1, p-value < 0.0005 including Yucatán specimens; X-squared = 48.4392, df = 1, p-value < 0.0005 excluding Yucatán specimens), (3) significantly more numerous along the Gulf of Mexico than along the west coast of Mexico, compared to reference specimens during spring migration (question 3; X-squared = 12.4593, df = 1, p-value < 0.0005), and (4) significantly more numerous below 200 m elevation (question 4; X-squared = 399.5081, df = 1, p-value < 0.0005).

Remote sensing

The EVI data extractions for Painted Bunting collection sites yielded an average of 10.4 pixels per location (range = 3–14). Locations near coastlines or on islands often had fewer pixels than inland site as the EVI data did not extend into water bodies. Extractions from random locations yielded an average of 11.1 EVI pixels (range: 4–16) and for the subset of reference specimen location data we got an average of 10.3 pixels (range: 3–14). After filtering, the reference EVI data consisted of a minimum of 1,939 values for each month from a minimum of 245 unique locations. For the real data, the number of unique locations ranged from 9 (in June) to 98, and the number of EVI values ranged from 11 (also in June) to 219.

For 10 months of the year, Painted Bunting collection sites in Mexico had higher EVI scores (i.e., higher primary productivity) than randomly generated locations within Mexico (p < 0.01; Fig. 4A). The only exceptions were May and June, when Painted Buntings are on their breeding grounds and are relatively scarce in Mexico. The highest monthly EVI average associated with the specimen data was from the month of October, which corresponds with high Painted Bunting densities in the states of Sinaloa and Sonora, where many if not most Painted Buntings undergo their annual molt (Rohwer, 2013). It is also in the month of October that we observed the greatest difference between the mean EVI value for collection sites and for random sites.

Comparison of EVI scores for Painted Bunting collection sites with those of other collecting sites indicated selection by the buntings for high productivity areas in only 5 months of the year (October, November, February, March, and April; Fig. 4B). In the months of July and September, EVI scores were significantly higher (p < 0.01) for the reference data. The discrepancies in the results from this analysis and the one based on random locations is likely due to a general collection bias toward highly-productive sites which are likely to have increased bird abundance and diversity.