Page  1 ï~~2004 THE MICHIGAN BOTANIST ECOLOGY OF EASTERN PRICKLY PEAR CACTUS (OPUNTIA HUMIFUSA) IN OAK OPENINGS PRESERVE, NORTHWESTERN OHIO Scott R. Abella* and John F. Jaeger Metroparks of the Toledo Area 5100 W. Central Ave. Toledo, OH 43615 ABSTRACT Opuntia humifusa (eastern prickly pear cactus) is listed as potentially threatened in Ohio, and we examined the characteristics of O. humifusa sites in Oak Openings Preserve in northwestern Ohio's Oak Openings region in an attempt to provide data that may help protect this species. Opuntia humifusa occurrences were associated with loose sands of the xeric Udipsamment Ottokee and Oakville soil series on sites that had been cleared before the 1940s during failed agricultural attempts. Shading by encroaching canopy trees is a threat to several O. humifusa populations in Oak Openings Preserve, and treatments that reduce canopy cover at these sites may help sustain this species and increase the proportion of flowering individuals. Because the patchy distribution of O. humifusa makes the species susceptible to local extinctions, the acquisition of sites by conservation organizations containing O. humifusa or providing suitable habitat is consistent with the perpetuation of this rare species in the Oak Openings region. Sandy sites previously disturbed by agricultural clearing, sand mining, or other soil disturbances should not be overlooked for their potential to provide O. humifusa habitat in this region. INTRODUCTION Opuntia humifusa (Raf.) Raf. (eastern prickly pear cactus) has a patchy but wide distribution in the eastern United States and southeastern Canada, ranging from Massachusetts through Wisconsin to southern Florida (Benson 1982). In the Great Lakes region, O. humifusa occurs in 10 counties in western lower Michigan (Voss 1985), southern Ontario including Point Pelee National Park (Reznicek 1982), four northern Ohio counties near Lake Erie and 12 southern Ohio counties (Cooperrider 1995), northern Indiana and Illinois near the southern tip of Lake Michigan (Swink & Wilhelm 1994), and scattered localities in southern Wisconsin (Benson 1982). Habitats of Opuntia humifusa in the Great Lakes region, based on herbarium records and published descriptions, vary widely (Noelle & Blackwell 1972). For example, Reznicek (1982) described two O. humifusa sites inland from Lake Erie in southern Ontario as low, south- and west-facing sandy ridges. In the Chicago region, O. humifusa occurs in Quercus savannas, old cemeteries on sandy soils that have been periodically mowed, and human-made limestone bar*Author for correspondence: sra8 @dana.ucc.nau.edu; present address: Ecological Restoration Institute, Northern Arizona University, Flagstaff, AZ 86011-5018

Page  2 ï~~THE MICHIGAN BOTANIST Vol. 43 rens (Swink & Wilhelm 1994). Kellerman (1901) reported that O. humifusa was common in open Quercus woods near Sandusky in northern Ohio, and this species also occurred in sand plains (Jennings 1908) and open fields (Moseley 1899) in the same region. Opuntia humifusa is listed as potentially threatened in Ohio (Ohio Division of Natural Areas and Preserves 2000). Regions supporting O. humifusa are widely disjunct in Ohio, and suitable habitats within these regions are patchy, making O. humifusa prone to local extinctions (Noelle & Blackwell 1972; Cooperrider 1995). Nonetheless, there are few detailed studies of the habitats and ecology of this species in the Great Lakes region and in the eastern United States in general. To help fill this gap in our knowledge in Ohio, made more serious by the potentially threatened status of O. humifusa, we studied O. humifusa habitats in Oak Openings Preserve in northwestern Ohio. The objective of this study was to document the environmental, plant community, and historical land-use characteristics of O. humifusa sites in Oak Openings Preserve in an attempt to provide data that may help protect this species. METHODS Study Species Nomenclatural history of Opuntia humifusa is convoluted (Noelle & Blackwell 1972). Gleason & Cronquist (1991) report that this species has been referred to as O. calcicola, O. compressa, O. opuntia, O. pollardii, O. rafinesquei, and O. vulgaris. Morphological characteristics of O. humifusa vary widely across its range, but authors in many regions have concluded that O. humifusa is a single species without varieties (Hanks & Fairbrothers 1969b; Voss 1985). This species often grows in clumps, and is typically 7.5-10 cm tall (Benson 1982). Flowering occurs in June and July (Cooperrider 1995), with yellow, showy flowers (Figure 1). Reproduction occurs both by seed and by the detachment of partial or full pads from a parent plant-these fragments readily root on soil surfaces (Voss 1985). Opuntia humifusa is a perennial and overwinters in its vegetative form, but no information was found in the literature as to the potential length of its life span. Opuntia humifusa often colonizes open, sandy, disturbed areas, and the species may be reduced or eliminated by shading during succession (Wallace & Fairbrothers 1987). Study Area Oak Openings Preserve is managed by the Toledo Area Metroparks and is located in Lucas County, northwestern Ohio (Figure 2). The preserve consists of a 1496-ha mosaic of wet prairies, open fields, conifer plantations, Quercus savannas, woodlands, and forests. Soils are sandy and are derived from beach dunes deposited during the Pleistocene at the western shoreline of Lake Warren, a glacial lake now partially occupied by Lake Erie (Moseley 1928). Presettlement vegetation in this region, based on 1821 land survey records, consisted of 51% Quercus velutina (black oak) and Quercus alba (white oak) savanna or barrens (< 43 trees ha-'), 23% Quercus woodland (> 43 trees ha-), and 27% treeless wet prairie (Brewer & Vankat 2001). Restoration of these native ecosystems is ongoing and is a high priority in Oak Openings Preserve (Abella et al. 2001). Data Collection The Toledo Metroparks maintains a continuously updated database of rare plant locations in Oak Openings Preserve based on formal botanical surveys and observations throughout the preserve. Opuntia humifusa occurs at eight known sites in Oak Openings Preserve, and because of the unique and distinctive appearance of O. humifusa these sites likely represent all or nearly all extant populations of this species in Oak Openings Preserve. We sampled each of these sites in May, July, and August 2002. At each site, we counted the number of Opuntia humifusa individuals and clumps. Distin

Page  3 ï~~2004 THE MICHIGAN BOTANIST 2004 THE MICHIGAN BOTANIST FIGURE 1. Aerial view of Opuntia humifusa flowering in Oak Openings Preserve, northwestern Ohio. (Photo courtesy of R.G. Jacksy, Toledo Area Metroparks).

Page  4 ï~~THE MICHIGAN BOTANIST Vol. 43 THE MICHIGAN BOTANIST Vol. 43 Southern Michigan FIGURE 2. Location of Oak Openings Preserve, Lucas County, northwestern Ohio (41033'N, 83Â~51'W). guishing individual O. humifusa is difficult because multiple pads can arise from the same root system (Ohio Division of Natural Areas and Preserves 2000). We defined and counted individual O. humifusa as a pad growing more than 30 cm from surrounding pads, and a clump as a cluster of O. humifusa individuals growing more than 1.5 m from surrounding clumps or individuals. We sampled the soils at each site to a depth of 130 cm using a bucket auger to confirm the soil series mapped for the site in the soil survey (Stone et al. 1980). The two series on which O. humifusa occurred, Ottokee and Oakville, are distinguished based on the presence (Ottokee) or absence (Oakville) of mottling within a depth of 100 cm (Stone et al. 1980). We determined Oi horizon thickness to the nearest cm around O. humifusa clumps using a ruler. Landforms at each site were described following descriptions in the soil survey (Stone et al. 1980). We measured canopy cover at each site using a densitometer (Geographic Resource Solutions, Arcata, CA) based on estimates to the nearest 5% cover. We also recorded the relative abundances of other plant species at each site, and potential threats to O. humifusa such as exotic species or shading. Plant nomenclature follows Voss (1972, 1985, 1996). Elevations of sites were obtained from a U.S. Geological Survey topographic map (Whitehouse quadrangle, 1964). To evaluate past land uses of the sites, we obtained 1939 aerial photographs (1:240,000 scale) of Oak Openings Preserve from the Natural Resources Conservation Service (Maumee, OH).

Page  5 ï~~2004 THE MICHIGAN BOTANIST RESULTS Characteristics of the eight Opuntia humifusa sites in Oak Openings Preserve are summarized in Table 1 and are described individually in the following sections. Numbers after each site name in the following sections correspond to the site's number in Table 1. Reed Plantation (1)-Associates of Opuntia humifusa at this site include Rubus flagellaris (northern dewberry), Fragaria virginiana (wild strawberry), Lepidium campestre (field peppergrass), Rumex acetosella (sheep sorrel), Antennaria spp., occasional Asclepias tuberosa (butterfly-weed), and seedlings of Acer rubrum (red maple), Prunus serotina (black cherry), Quercus velutina, and Sassafras albidum (sassafras). Canopies consist of ca. 20-cm diameter Quercus velutina, Quercus palustris (pin oak), Pinus strobus (eastern white pine), and Pinus banksiana (jack pine). The site consists of an opening adjacent to the south of a Pinus banksiana plantation and north of an Acer rubrum-dominated forest on a different soil series (Tedrow, a moist series [Stone et al. 1980]). Few O. humifusa at this site flowered, and threats to this population appear to be shading by an encroaching canopy of Quercus and Pinus, smothering by leaf litter, and the presence of an invasive shrub Elaeagnus umbellata (autumn olive). Yucca Meadow (2)-This site has been restored to Quercus savanna by the thinning of Quercus velutina and the removal of Acer rubrum. Pinus resinosa (red TABLE 1. Summary of characteristics of Opuntia humifusa sites in Oak Openings Preserve, northwestern Ohio Site 1 2 3 4 5 6 7 8 No. Opuntia clumps 20 18 1 2 9 15 2 5 No. Opuntia individuals 69 61 13 3 28 79 10 32 Size Opuntia area (m2)1 6000 2400 100 50 400 1000 100 100 Landform Dune Dune Dune Dune Dune Dune Beach Beach type knoll knoll knoll ridge knoll knoll ridge ridge Elevation (m) 215 217 216 219 215 215 215 215 Soil series2 Ottokee Oakville Oakville Oakville Oakville Ottokee Oakville Ottokee Oi horizon Patchy3 Absent Patchy Absent Patchy Absent Absent Patchy Canopy cover (%)4 50 <5 <5 0 50 50 0 0 1939 land Agri- Agri- Agri- Sand Agri- Agri- Agri- Agriuse culture culture culture dune culture culture culture culture 1 Size of area containing Opuntia including area between clumps. 2 Ottokee and Oakville series classified as mixed, mesic Aquic and Typic Udipsamments (Stone et al. 1980). 3 Patchy = ranges from absent to a maximum of 4 cm thick across site. 4 Average of site or point-sample above Opuntia for small-sized sites.

Page  6 ï~~THE MICHIGAN BOTANIST Vol. 43 pine) plantations are adjacent to this site to the west, and the rest of the site is surrounded by closed-canopy Quercus forest. Andropogon scoparius (little bluestem), Krigia virginica (dwarf-dandelion), Lupinus perennis (wild lupine), Rubus flagellaris, Lespedeza capitata (bush clover), Fragaria virginiana, Asclepias tuberosa, and occasional Yucca filamentosa (yucca) dominate this site. Encroachment by the exotic Elaeagnus umbellata is a possible threat to this population of Opuntia humifusa. Vasvery Homestead (3)-This site is adjacent to a private inholding to the north, a road and a Pinus strobus plantation to the west, and a restored Quercus savanna to the south and east. Common plants near Opuntia humifusa at this site include Rubus flagellaris, Euphorbia corollata (flowering spurge), Rhus copallina (winged sumac), Lespedeza capitata, and seedlings of Quercus velutina. Two other state-listed plants, Asclepias amplexicaulis (blunt-leaf milkweed) and Prunus pumila (sand cherry) occur within 100 m of O. humifusa at this site. Because of its proximity to a private inholding, the area where O. humifusa occurs at this site was not included in restoration treatments that were applied to adjacent areas, and threats to this population of O. humifusa include shading by encroaching canopy trees and brush. Railroad Ridge (4)-Common plants around Opuntia humifusa at this site include Quercus velutina seedlings, Carex spp., Rubus flagellaris, Euphorbia corollata, Rumex acetosella, Lepidium campestre, Asclepias tuberosa, Asclepias syriaca (common milkweed), Krigia virginica, Lespedeza capitata, Ambrosia artemisiifolia (common ragweed), and Conyza canadensis (horseweed). This site comprises the highest elevation of all O. humifusa sites, and soils consist of loose, shifting sand. A bike trail is located 30 m north of the site, and this trail occupies an old railroad bed present in 1939. The site was an open sandy area in 1939, and is the only O. humifusa site not in agriculture at that time (Table 1). Removal of O. humifusa by park visitors is a potential threat to O. humifusa at this site because of its proximity to the trail, although there was no present evidence that any O. humifusa have been recently removed. Jack Pine Opening (5)-This site consists of an opening within a Pinus banksiana plantation. Canopy trees include Quercus palustris and Quercus velutina, and ground-flora includes Rubus flagellaris, Krigia virginica, Rumex acetosella, Rhus copallina, Yucca filamentosa, and seedlings of Quercus velutina, Quercus palustris, and Sassafras albidum. Potential threats to this population of Opuntia humifusa are shading by encroaching canopy trees and smothering by leaf litter. Douglas-Fir Border (6)-Adjacent to the east of a Pseudotsuga menziesii (Douglas-fir) and Picea abies (Norway spruce) plantation, Opuntia humifusa on this site occur in an opening surrounded by Quercus saplings (Figure 3). Associates of O. humifusa include Pteridium aquilinum (bracken fern), Lepidium campestre, Andropogon scoparius, and Quercus velutina seedlings. Shading by

Page  7 ï~~2004 THE MICHIGAN BOTANIST 2004 THE MICHIGAN BOTANIST FIGURE 3. Opuntia humifusa clump (left foreground) in an opening adjacent to a Pseudotsuga menziesii and Picea abies plantation established in 1950, Oak Openings Preserve, northwestern Ohio. Shading by encroaching canopy trees is a potential threat to O. humifusa at this site and several other sites in Oak Openings Preserve. (Photo by S.R. Abella, 11 May 2002). encroaching Quercus saplings and height growth of conifers in the plantation are potential threats to O. humifusa at this site. Girdham Field (7)-This site is 50 m southeast of a Pinus resinosa and Pinus strobus plantation and is part of a 12-ha meadow with occasional large Quercus alba that has been restored from closed-canopy Quercus and Acer rubrum forest. Other species occurring near Opuntia humifusa include Panicum clandestinum (deertongue), Rubus flagellaris, Potentilla simplex (common cinquefoil), Fragaria virginiana, and Rumex acetosella. There are no apparent threats to this O. humifusa population. White Oak Savanna (8)-A 122-cm diameter open-grown Quercus alba occurs within 50 m of the Opuntia humifusa clumps at this site that is part of the same meadow as the Girdham Field site (Figure 4). Aerial photographs taken in 1939 indicate this site was cleared for agriculture at that time, but the large Q. alba is visible in the photograph and was apparently not removed during agricultural clearing. Common plants around O. humifusa at this site include Rubus flagellaris and Ambrosia artemisiifolia. No imminent threats to O. humifusa are apparent at this site.

Page  8 ï~~THE MICHIGAN BOTANIST Vol. 43 THE MICHIGAN BOTANIST Vol. 43 FIGURE 4. White oak savanna Opuntia humifusa site characterized by a 122-cm diameter opengrown Quercus alba, Oak Openings Preserve, northwestern Ohio. Opuntia humifusa at this site occurs in clumps scattered around the Q. alba. (Photo by S.R. Abella, 4 August 2002). DISCUSSION Habitats of Opuntia humifusa Occurrences of Opuntia humifusa in Oak Openings Preserve are associated with the xeric Oakville and Ottokee soil series, occupying the highest elevations in the preserve on dune knolls, dune ridges, and beach ridges. However, only a small areal portion of these series support O. humifusa, and many apparently suitable sites were unoccupied by O. humifusa. It is unclear what factors constrain the distribution of O. humifusa within areas of the Oakville and Ottokee soils. Consistent with a study of O. humifusa habitats in New Jersey (Hanks & Fairbrothers 1969a), there does not appear to be a distinct plant community in which O. humifusa occurs in Oak Openings Preserve. Plant assemblages associated with O. humifusa varied by site, with Rubus flagellaris exhibiting the highest constancy (87%) at O. humifusa sites. Attempts to locate additional O. humifusa populations in Oak Openings Preserve, if they exist, could focus on open areas of loose sand of the Oakville and Ottokee series, areas that have been disturbed by agricultural clearing or other disturbance, and areas supporting other plant species characteristic of dry, open environments. Seven of eight Opuntia humifusa sites in Oak Openings Preserve were in

Page  9 ï~~2004 THE MICHIGAN BOTANIST agriculture in 1939, suggesting O. humifusa was present before clearing and the plants or seed survived, or O. humifusa did not occur on these sites before clearing and became established sometime after farm abandonment. It is possible that soil disturbances created by agricultural clearing provided a favorable environment for O. humifusa colonization. Many of the abandoned farms were converted to Pinus plantations in the 1940s and 1950s when land for Oak Openings Preserve was acquired by the Toledo Metroparks (Abella & MacDonald 2002). Because all eight presently known O. humifusa sites occur within 100 m of a conifer plantation, it is uncertain if some O. humifusa sites were lost by the conversion of abandoned farms to plantations. Origin and Distribution of Opuntia humifusa The origin of Opuntia humifusa in the Oak Openings region is unclear. In Wood County, 13 km east of the city of Bowling Green and 35 km southeast of Oak Openings Preserve, Moseley (1931) documented an O. humifusa occurrence on a site known to have been a long-term Native American campsite. Moseley (1931) also noted that O. humifusa occurrences around Sandusky in northern Ohio east of the Oak Openings region were associated with the presence of Native American artifacts. He postulated that Native Americans had introduced O. humifusa to northern Ohio because they favored its edible, succulent fruit. In Moseley's classic paper (1928) on the flora of the Oak Openings region based on his botanical surveys in the 1890s and early 1900s, he does not mention O. humifusa as occurring in the region. Moseley's routes through Oak Openings are uncertain, and there could be many reasons why he did not document the occurrence of O. humifusa if the species did occur in the Oak Openings region at that time. Noelle & Blackwell (1972) reported that the earliest known herbarium record of O. humifusa in Ohio other than for the Sandusky region is a collection in 1911 in Adams County in extreme southern Ohio. However, Noelle & Blackwell (1972) asserted that the absence of herbarium records for O. humifusa should be interpreted cautiously because of the scattered distribution of O. humifusa and the incompleteness of early collection records. The first published documentation of O. humifusa in the Oak Openings region appears to be by Easterly (1979) during his rare plant survey. It is uncertain how O. humifusa became established in the Oak Openings region and for how long the species has been in this region. Protection of Opuntia humifusa Shading has been widely cited to reduce flowering and eventually eliminate Opuntia humifusa (Hanks & Fairbrothers 1969a; Reznicek 1982; Wallace & Fairbrothers 1987). Five of eight O. humifusa sites in Oak Openings Preserve exhibited encroachment by trees or shrubs, and shading appears to be an imminent threat to these O. humifusa populations. Restoration treatments that restore the open Quercus savanna vegetation native to O. humifusa sites (Abella et al. 2001) would probably alleviate shading threats to O. humifusa and increase the proportion of flowering individuals. Continued monitoring of these sites is necessary to ascertain the temporal dynamics of O. humifusa. Although the presettlement distribution of O. humifusa in Oak Openings Preserve is not known, the

Page  10 ï~~10 THE MICHIGAN BOTANIST Vol. 43 present fragmented nature of the preserve and the localized occurrences of O. humifusa suggest that establishing O. humifusa on additional sites in Oak Openings Preserve might be desirable. Opuntia humifusa can be established by removing pads from existing plants and planting the pads (Voss 1985). Because of the potentially threatened status of O. humifusa in Ohio, the acquisition of sites by conservation organizations containing O. humifusa or providing suitable habitat in the Oak Openings region is consistent with the perpetuation of this rare species in Ohio. Results of this study suggest that sandy sites disturbed by agricultural clearing, sand mining, or other soil disturbances should not be overlooked for their potential to provide O. humifusa habitat in the Oak Openings region. ACKNOWLEDGEMENTS We thank Denise Gehring, Bob Jacksy, Jenny Finfera, Monique Beans, Chris Ferree, Karen Menard, Heather Norris, Mark Plessner, Kathryn Nelson, Sarah McCallum, Kim High, and others with the Toledo Metroparks for monitoring rare plant species in Oak Openings Preserve. Jenny Finfera and Bob Jacksy maintain the rare plant database. We also thank Neil MacDonald and Jenny Finfera for reviewing the manuscript. LITERATURE CITED Abella, S.R., J. F. Jaeger, D. H. Gehring, R. G. Jacksy, K. S. Menard, & K. A. High. 2001. Restoring historic plant communities in the Oak Openings region of northwest Ohio. Ecological Restoration 19: 155-160. Abella, S. R., & N. W. MacDonald. 2002. Spatial and temporal patterns of eastern white pine regeneration in a northwestern Ohio oak stand. Michigan Botanist 41: 115-123. Benson, L. 1982. The cacti of the United States and Canada. Stanford University Press, Stanford, California. 1044 pp. Brewer, L. G., & J. L. Vankat. 2001. The vegetation of the Oak Openings of northwest Ohio at the time of Euro-American settlement. Map and text. Ohio Biological Survey, Columbus, Ohio. Cooperrider, T. S. 1995. The Dicotyledoneae of Ohio. Part 2. Linaceae through Campanulaceae. Ohio State University Press, Columbus, Ohio. 656 pp. Easterly, N. W. 1979. Rare and infrequent plant species in the Oak Openings of northwest Ohio. Ohio Journal of Science 79: 51-58. Gleason, H. A., & A. Cronquist. 1991. Manual of vascular plants of northeastern United States and adjacent Canada. New York Botanical Garden, Bronx, New York. 910 pp. Hanks, S., & D. E. Fairbrothers. 1969a. Habitats and associations of Opuntia compressa (Salisb.) Macbr. in New Jersey. Bulletin of the Torrey Botanical Club 96: 592-596. Hanks, S. & D. E. Fairbrothers. 1969b. Diversity of populations of Opuntia compressa (Salisb.) Macbr. in New Jersey. Bulletin of the Torrey Botanical Club 96: 641-652. Jennings, O. E. 1908. An ecological classification of the vegetation of Cedar Point. Ohio Naturalist 8: 291-340. Kellerman, W. A. 1901. Notes on the flora of Sandusky. Ohio Naturalist 1: 82-85. Moseley, E. L. 1899. Sandusky flora. Ohio Academy of Science, Special Paper Number 1. 167 pp. Moseley, E. L. 1928. Flora of the Oak Openings. Proceedings of the Ohio Academy of Science, Volume 8, Special Paper Number 20: 79-134. Moseley, E. L. 1931. Some plants that were probably brought to northern Ohio from the west by Indians. Papers of the Michigan Academy of Science, Arts and Letters 13: 169-172. Noelle, H. J., & W. H. Blackwell. 1972. The Cactaceae in Ohio. Castanea 37: 119-124. Ohio Division of Natural Areas and Preserves. 2000. Rare native Ohio plants: 2000-01 status list. Ohio Department of Natural Resources, Columbus, Ohio. 28 pp. Reznicek, A. A. 1982. The cactus in southwestern Ontario. Ontario Field Biologist 36: 35-38.

Page  11 ï~~2004 THE MICHIGAN BOTANIST 11 Stone, K.L., E.H. McConoughey, G.D. Bottrell, & D.J. Crowner. 1980. Soil Survey of Lucas County, Ohio. U.S. Department of Agriculture, Soil Conservation Service. U.S. Government Printing Office, Washington, D.C. 139 pp. Swink, F., & G. Wilhelm. 1994. Plants of the Chicago region. Indiana Academy of Science, Indianapolis, Indiana. 921 pp. Voss, E.G. 1972. Michigan Flora. Part I. Cranbrook Institute of Science, Bloomfield Hills, Michigan. 488 pp. Voss, E.G. 1985. Michigan Flora. Part II. Cranbrook Institute of Science, Bloomfield Hills, Michigan. 727 pp. Voss, E.G. 1996. Michigan Flora. Part III. Cranbrook Institute of Science, Bloomfield Hills, Michigan. 622 pp. Wallace, R. S., & D. E. Fairbrothers. 1987. The New England distribution of Opuntia humifusa (Raf.) Raf. Rhodora 89:327-332.