Distribution, diversity, and traits of native, exotic, and invasive climbing plants in Michigan ROBYN J. BURNHAM AND CRISTINE V. SANTANNA Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109-1079, USA; e-mail: [email protected]; e-mail:

Abstract. We compiled records of all the known climbing plant species both native and nonnative in the state of Michigan, USA. County-level distributions and a broad suite of traits related to ecological and reproductive success were individually scored for each species. Nonnative climbing species were subdivided and classified as either invasive or exotic. A total of 103 climbing species are present in the state, 50% of which are native. We classified only ten climbing species as currently invasive: of those 40% are woody, compared to 31% woody native and 33% woody exotic species. Our research asks whether latitude is correlated with either species richness or mode of dispersal among climbers. We also asked whether sexual system, dispersal mode, and unit of dispersal are different in native versus non-native climbers, and whether the dispersal mode of common trees is different from that of common climbers. We found latitudinally bimodal species richness for all classes of climbers, which we propose is due to collecting effort, growing season length, and human population density. We found surprisingly high numbers of climbing species at northern latitudes, in spite of harsh winter conditions, especially for climbing plants whose vascular tissues are compromised by freezing temperatures. Native species are significantly more often dioecious (27%) than non-natives (6%); however one of the woody invasive species, Celastrus orbiculatus, is functionally dioecious. Collectively, climbers include more abiotically dispersed species (62%) than biotically dispersed (38%). However, the 18 most common native species (found in more than 40 of 83 counties) are 61% biotically dispersed. Native woody climbers are 81% biotically dispersed, whereas native trees include 38–40% biotically dispersed species. Native climbing species are more often dispersed as fruits (52%) than are non-native climbers (37%), which are more often dispersed as seeds. Climbing mechanism is generally achieved by stem apical twining in both native and non-native species; however when tendrils are produced, native species produce similar proportions of leaf, petiole, and axillary tendrils, while nonnative species largely produce leaf tendrils, a mechanism that is phylogenetically concentrated in the crop and crop-weed family, Fabaceae. Based on traits of the ten currently invasive climbing species in Michigan, we identify ten exotic species that are most likely to become invasive, most of which are perennials, hermaphroditic, with abiotically dispersed fruits, and modified climbing organs. Climbing species add significantly to biodiversity in Michigan, comprising 3.6% of the 2858 vascular plants. Climbing guilds in the temperate zone are more morphologically diverse and species rich than broadly recognized. Key Words: Common species, dispersal, latitudinal diversity, liana, plant guild, species richness, vine.

In the western hemisphere, climbing plant species are found in ecosystems from the southern Arctic to Patagonia (Gentry, 1991a; Johnson, 2001; Zuloaga et al., 2008; Carrasco-Urra & Gianoli, 2009). It is widely observed that species of vines and lianas (hereafter Bclimbers^) comprise a larger proportion of tropical floras than of

temperate floras (Gentry, 1991a; Schnitzer & Bongers, 2002; Schnitzer, 2005; Gallagher et al., 2011; Jiménez-Castillo & Lusk, 2013). Given that tree species richness in temperate regions is also lower per area than in tropical regions, the generalization may merit reevaluation. To our knowledge, Michigan climbers have previously been

Brittonia, DOI 10.1007/s12228-015-9385-1 ISSN: 0007-196X (print) ISSN: 1938-436X (electronic) © 2015, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A.

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treated at small scales, or with reference to a phylogenetically restricted group of species (e.g., Harper, 1918; Billington, 1943; Gysel, 1951; Wells & Thompson, 1972; Parker & Schneider, 1975; Barnes & Wagner, 1992; Tibbetts & Ewers, 2000; Leicht-Young et al., 2010; Pavlovic & Leicht-Young, 2011; Fan et al., 2013). Our research in Michigan, USA provides an opportunity to evaluate all species of the climbing plant guild across a temperate region spanning several climatic zones, more than 250,000 km2, and including wide habitat breadth. Interactions between climbing plants and other life forms can be both beneficial and detrimental, depending on the species and the interactions. Climbers in most ecosystems add food resources for birds, mammals, insects, and fungi. Their branches provide cover and nesting habitats for a variety of insects and birds, as well as trackways for small mammals. In disturbed sites, climbers have been planted to slow erosion, and these effects probably occur in natural forest openings as well (Forseth & Innis, 2004; Ladwig & Meiners, 2010a). Climbers are implicated, however, in collateral damage to trees when harvesting practices do not include prior cutting of woody climbers (Pérez-Salicrup, 2001; Gerwing & Uhl, 2002; Grauel & Putz, 2004; Pavlovic & Leicht-Young, 2011). The ensuing multiple-tree falls create forest gaps larger than those caused by single-tree harvesting. Gaps formed by anthropogenic or natural disturbance may be colonized by climbers that create shade, impeding tree regeneration and seedling emergence and stalling forest regrowth (e.g., ^Montane Grape Vine Openings;^ DeFelice, 2002; Madden et al., 2004; Cushman & Gaffney, 2010; Miller et al., 2010; Harris & Gallagher, 2010). Leaves of high-climbing lianas shade the leaves of host trees, depressing tree photosynthesis and accelerating the decline of trees that are already struggling (Ingwell et al., 2010). Tree saplings can be girdled by apically twining climbers, which especially impacts tree phloem flow (Lutz, 1943). The relatively uncommon parasitic climbers, like Cuscuta spp., can suppress host vegetation by exporting water and nutrients for their own growth (Farah & AlAbdulsalam, 2004; Lanini & Kogan, 2005; Zaroug et al., 2014). In cool temperate climates, lianas can increase the volume of accumulated ice on tree branches in winter, causing increased susceptibility to host breaking and toppling (Siccama et al., 1976). There is undoubtedly a competitive

effect underground for nutrients, water, and fungal interactions, but this has received substantially less attention (Dillenburg et al., 1993a, 1993b, 1995). An interesting idea, proposed by Yanoviak (2013), is that trees may be protected from lightning strikes by lianas extending through and above their canopies, however this is rarely documented. We posed the following testable hypotheses on the distribution and characteristics of climbing species in Michigan. We predict that climber species richness decreases linearly with increasing latitude, due to decreasing mean annual temperature. We expect that this is true for native species as well as non-native species (both invasive and exotic). BExotic^ includes species introduced outside of their historic range, even if native to North America outside of Michigan. We predict fewer dioecious and more hermaphroditic species among non-native than among native species. Dioecious species require two individuals for reproduction, so among colonizers, dioecy is less likely than monoecy or hermaphroditism (Baker, 1955, Herron et al., 2007). We predict that a larger proportion of both monoecious and hermaphroditic species will be found among non-native species than among native species because of the potential for reproduction from a single colonizer. We predict that more native climbing species bear animal dispersed fruits than do non-natives, but that animal dispersal is more frequent among invasive species than exotics. We predict that woody climbers (lianas) include more animal dispersal than trees in Michigan, contrary to the pattern in tropical floras. Lianas have been characterized as more often wind dispersed than co-occurring tree species, but only rarely has it been noted that this is not the case for temperate climbing species (Gentry 1991b). We predict that a large proportion of non-native climbers are annual species or herbaceous perennial species, both of which overwinter without requiring xylem innovations to survive freezing temperatures. We predict that the distribution of climbing mechanisms (twiners, tendrils, hooks, etc.) is similar among native and non-native species.

Here, we map the geographic distribution of species richness among climbers, and synthesize data from six degrees of latitude using collection records dating prior to and during the current temperature and atmospheric CO2 increase. We compare traits across three classes of climbing species in Michigan and explore the possibility that traits present in invasive species can help predict future range expansion in currently noninvasive species.

Methods We compiled data on all species of climbers (herbaceous and woody) currently growing

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naturally outside of cultivation in the state of Michigan (complete list, Appendix). Climbers were defined as species capable of growing at least 1m long, not fully self-supporting, and regularly using other plants or structures to achieve height. We excluded species that root regularly at nodes without normally climbing higher than 0.5 m (e.g., Bartonia paniculata (Michx.) Muhl., Mitchella repens L.), arching shrubs, and ground-cover scramblers (e.g., most species of Rosa L. and Rubus L.). One species hybrid developed by plant breeders escapes in Michigan (Michigan Invasive Plants Council), but is not included in our analyses: Ipomoea × multifida (Raf.) Shinners. We include a single species each of Galium L. and Rosa, which clearly fulfill the criteria above. Climber species were classified as either native or non-native. Non-natives were further subdivided into currently invasive or noninvasive (hereafter Bexotic^) in Michigan. Candidacy for invasive status was based on a listing in one or more of the resources in Table I. We determined the current county-level geographic extent of non-native species in Michigan using the Michigan Flora Online (2011 and onwards). Our final criterion for classifying non-native species as invasive or exotic was based on either documented status as invasive in Michigan, or on recent county-level range expansion documented by comparison of range maps in Voss (1972, 1985, 2004) with current county distributions. For example, although both Humulus japonicus Siebold & Zucc. and Pueraria montana (Lour.) Merr. are reported in the state and they are classified as invasive in other states, the current geographic extent in Michigan is limited (1–4 counties) and there is no evidence of recent range expansion, so they are classified as exotic rather than invasive. Some resources listed in Table I list species as invasive because of their potential for

invasion, as documented elsewhere, although they are not yet recorded in the state (e.g., Persicaria perfoliata (L.) H. Gross); we counted these as neither present nor invasive. Our database of both climbing and scrambling species includes 85 traits scored on 123 climbing and scrambling species found in Michigan and is available on the CLIMBERS web site (http:// climbers.lsa.umich.edu/). For the analyses here, we limited the species treated to the 103 species bearing clear climbing mechanisms, such as adventitious roots, tendrils of all types, apical twining, and recurved spines, but excluded all species that scramble without achieving a truly dependent habit. We selected the following characters from the database for analysis: sexual system (hermaphrodite, monoecious, dioecious), dispersal mode (biotic, abiotic), dispersal unit (fruit, seed), habit (woody, herbaceous), life span (annual, biennial, perennial), and climbing mechanism. Geographic range in Michigan was determined based on floristic literature (Billington, 1943; Voss, 1972, 1985, 2004; Voss & Reznicek, 2012), herbarium voucher specimens, personal vouchered collections, and the continuously updated Michigan Flora Online (http://www.michiganflora.net/ home.aspx). Herbarium collections of Michigan flora date from the 1860s, and we have assumed that species now absent in areas of intense human activity are represented among older herbarium collections, at least at the county-level. SPECIES RICHNESS AND LATITUDE BANDS

County boundaries in the lower peninsula of Michigan were originally defined as comprising 16 townships; almost all of the 68 lower peninsula counties were thus delimited (Welch, 1972). These county boundaries (Fig. 1) apportion roughly equal areas, ranging from 850 to 2500 km2 per county (mean = 1538km2, s.d.= 328). In the upper peninsula (15 counties), county size ranges from

TABLE I DATA SOURCES FOR INVASIVE SPECIES CLASSIFICATIONS. 1 2 3 4 5 6

Michigan Department of Natural Resources Invasive Guide, MI DNR (http://mnfi.anr.msu.edu/invasive-species/ InvasivePlantsFieldGuide.pdf) University of Michigan Herbarium, Michigan Flora website listing as widespread and a ‘weed’, or ‘potentially invasive’. (http://www.michiganflora.net/home.aspx) Midwestern United States at Midwest Invasive Plant Network (MIPN: http://mipncontroldatabase.wisc.edu/) Midwest Invasive Species Network (http://www.misin.msu.edu/) Michigan Department of Agriculture and Rural Development: Prohibited or Restricted Noxious Weeds List (http:// www.michigan.gov/mdard/0,4610,7-125-239041275-149078–,00.html) MIPC – Michigan Invasive Plant Council; 6 of 40 plants listed are climbing (http://invasiveplantsmi.org/index.html)

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FIG. 1. Michigan political map, showing county names and human population density per square mile, as reported by the Michigan Department of Technology, Management and Budget (http://www.michigan.gov/cgi/). Horizontal lines to right indicate approximate southern limit of latitude bands.

1400 to 4700 km2 (mean = 2835km2, s.d. = 802). In the lower peninsula 60 of 68 counties are less than 2000 km2, while 13 of 15 upper peninsula counties are larger than 2000 km2, including two counties over 4000 km 2 . However, no correlation exists between county size and number of climbing species in the upper, lower, or combined peninsulas (r2 < 0.01, p = 0.81, 0.55, and 0.88 for native, non-native, and all species, respectively), so we did not scale species richness by county size. In fact, the smallest county,

Benzie (832 km2), has a higher than average species richness across all categories of climbers (n = 43 species). By using readily available county-level data, we were able to calculate an average number of climber species per county and a climber richness for 13 latitudinally constrained Bbands^ of counties (2 in the upper peninsula and 11 in the lower), allowing for roughly uniform area comparisons (Figs. 1, 2). Latitude bands included counties whose southern boundaries occur at the same latitude; bands are referred

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FIG. 2. Michigan climber richness in number of species, with quartile breaks for richness scale for each panel (note that coding is not equivalent among panels). A. All species. B. Invasive species only. C. Native species only. D. Non-native species (exotic + invasive) only.

to by that southern latitude limit. Habitats in Michigan include oak savannas, prairies, wet and mesic deciduous hardwood forests, mixed hardwood and deciduous forests, fens, bogs, coastal dunes, jack pine forests, and boreal forests, creating broad habitat heterogeneity across each latitudinal band. The range of habitats included at a single latitude band is broader than for any single county. Habitat-restricted species

(especially coastal dune species) are often found in only one or two counties per latitude band. SPECIES TRAITS OF NATIVES AND NON-NATIVES

Michigan climber species were classified as biotically (mammal, bird, insect) or abiotically (wind, water, ballistic, gravity) dispersed. Species were coded based on literature or direct evidence

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of a dispersal mechanism on the fruit or seed. Species with fleshy fruits or seeds were coded as biotically dispersed. Abiotically dispersed species bear a plume or wing (wind dispersed) or bear neither lofting agent nor fleshy attractant (gravity, ballistic, or water). Climbers chosen for comparison to trees were the 34 species (16 native, 18 non-native) with a persistent woody above ground stem or woody overwintering caudex. To generate tree lists, we used the U.S.D.A. Forest Service tree atlas (http://www.nrs.fs.fed.us/atlas/) of 134 tree species that occur east of the 100th meridian. From these, we selected species present in Michigan. The atlas also includes data on tree dispersal, which we used to generate scores for biotic / abiotic dispersal mechanism, based on the same criteria used for climbers. Michigan climbers were classified into one of four sexual systems (Appendix): hermaphrodite, monoecious, dioecious, and other (including unclassified species and polygamous species with mixed hermaphroditic and unisexual flowers). They were also classified as bearing one of seven climbing mechanisms: simple apical twiner, leaf-modified tendril, petiole-modified tendril, adventitious roots, spine/hooks, axillary tendril, and suction holdfasts. A few species bear more than one climbing mechanism (e.g., Parthenocissus quinquefolia); we classified climbing in such species as the single method anchoring the plant most firmly to its host. Differences in the proportions of binary trait variables between groups of climbers were tested using the Z statistic, reporting p values. To test equivalence among mean values for quantitative traits, we applied single factor ANOVA and Tukey-HSD tests, with significance levels of p = 0.05. For ordinal variables we applied chi-square tests of significance and report p values. For latitudinal correlation with species richness, we performed linear and quadratic regressions based on county-level and on latitude-band richness values, reporting r2 and p values. We compared the residuals of the resulting regressions to evaluate the importance of mid-latitude richness values. Results FAMILY COMPOSITION AND NATIVE STATUS

We recorded 103 species of native or naturalized climbing plants in Michigan as of December,

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2014 (Appendix). Fifty-one species are native to Michigan, while 52 have been introduced since the early 1800s. The climbers comprise 24 angiosperm families and one fern (Lygodium palmatum (Bernh.) Swartz). Of the 52 non-native species, we classify 10 as invasive and 42 as exotic (currently non-invasive). Sixteen angiosperm families and one fern are represented by native species, nine families are represented by invasive species, and 14 families are represented by exotic species. Among non-natives, 18 species (2 invasive, 16 exotic) are members of the Fabaceae (35%), while only 11 (22%) native species are in the Fabaceae. Similarly, seven species of Cucurbitaceae are among non-natives and only two are present among natives. Almost half (48%) of the nonnative climbing species represent these two crop-rich families. While only ten species are currently invasive in Michigan, these ten can individually or in combination produce significant environmental threats (Banasiak & Meiners, 2009; Jesse et al., 2010; Horton & Francis, 2014; Molano-Flores, 2014). The 103 climbing species represent 3.6% of the 2858 vascular plants recognized in the Michigan flora (Voss & Reznicek, 2012) and the 102 climbing angiosperms comprise 3.7% of the 2727 Michigan angiosperms. The 51 native climbing species represent 2.8% of the 1808 native vascular plant species, and the 52 non-native climbers represent 4.9% of all non-natives (complete flora values from Michigan Flora Online). LATITUDINAL DISTRIBUTION OF SPECIES RICHNESS: NATIVE CLIMBING SPECIES

Native species richness per county decreases significantly from south to north (Fig. 3, Table II), with southern counties including up to 40 native climbing species (Berrien county) and northern counties (>43.5° N latitude) including no more than 23. Both single county richness (Fig. 3A) and latitudeband richness (Fig. 3B) are negatively correlated with latitude (county richness × latitude r2 = 0.300, p < 0.001; latitude-band richness x latitude r2 = 0.649, p <0.001). Southern latitude-band richness reaches 45 native species while northern latitude-bands (>43.5°N) show no more than 28 natives. Between 43.5°N and 44.5°N, native species richness range is 2–22 species per county (mean =

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FIG. 3. Species richness shows significant negative correlations with latitude for all climbers, native climbers, and non-native climbers. See Table II for all correlation coefficients. A. County level species richness, only linear regressions shown. B. Latitudinal band species richness, each band combines 5–8 counties; linear and polynomial regressions shown.

9.8, s.d.= 5.43), and 19–26 species per latitude-band. Only three of the 23 counties at this mid-latitude have > 15 native species. In contrast, in the upper peninsula at 45.5°N and 46.14°N, counties show higher average native species richness (16.6 and 15.8 species,

respectively; s.d. = 3.5 and 4.9). There, native species richness per latitude-band is 28 and 25 species at 45.5 and 46.14°N, respectively. Although bands and counties in the lower peninsula are smaller, no linear correlation with climber richness was found.

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TABLE II LINEAR AND QUADRATIC REGRESSIONS OF SPECIES RICHNESS × LATITUDE AT COUNTY AND LATITUDE-BAND SCALES.

All Species per county (n=103) Native Species per county (n=51) Non-Native Species per county (n=52) Invasive Species per county (n=10) All Species per band (n=103) Native Species per band (n=51) Non-Native Species per band (n=52) Invasive Species per band (n=10)

Linear Regression

2nd Order Polynomial (quadratic)

y = -4.2843x + 212.01 R2 = 0.234 y = -3.289x + 161.4 R2 = 0.288 y = -0.996x + 50.64 R2 = 0.083 y = -0.495x + 26.34 R2 = 0.113 y = -8.3388x + 413.29 R2 = 0.538 y = -5.0194x + 250.43 R2 = 0.679 y = -3.3206x + 162.86 R2 = 0.306 y = -0.5872x + 33.334 R2 = 0.243

y = 3.2965x2 – 292.59x + 6509.3 R2 = 0.446 y = 2.2367x2 – 198.9x + 4433.9 R2 = 0.507 y = 1.0598x2 – 93.686x + 2075.4 R2 = 0.227 y = 0.4294x2 – 38.06x + 847.17 R2 = 0.253 y = 4.1711x2 - 373.52x + 8398.3 R2 = 0.781 y = 1.7954x2 – 162.21x + 3687.5 R2 = 0.836 y = 2.3757x2 – 211.32x + 4710.9 R2 = 0.589 y = 0.5489x2 – 48.646x + 1084.2 R2 = 0.628

LATITUDINAL DISTRIBUTION OF SPECIES RICHNESS: NON-NATIVE CLIMBING SPECIES

Non-native climbing species also show a pattern of decreasing species richness with increasing latitude (Fig. 3, Table II). At the county scale, the linear relationship is significant, but not strong (p < 0.01, r2 = 0.078), with a lower slope than for native species. In the northern-most latitude band (46.14°N), eight of the ten invasive species are present, with three to six (mean = 5.0, s.d. = 1.0) present in each county. Of the 42 exotic species, only 10 are present in the northernmost latitude band, with 1 to 6 per county (mean = 3.1, s.d. = 1.7). Conversely, in the four southern latitude bands, non-native species comprise 37 to 45% of all climbing species per band and up to 43% per county (1–26 species per county). The largest number of non-natives is found in Washtenaw county, with nine invasives and 17 exotics. Three central latitude-bands (43.5 to 44.3°N) harbor only 7, 7, and 11 non-native species respectively, with individual counties averaging 3.7 non-natives (s.d. = 2.0, range: 1–10, Fig. 2D). In isolation, the small number of invasive species limits interpretation of a trend, however the pattern shadows the exotic species: a shallow slope, decrease in richness at 43 to 45°N latitude, and a rebound at 45.5°N (Fig. 3). LATITUDINAL DISTRIBUTION OF SPECIES RICHNESS: ALL SPECIES AND BI-MODAL RICHNESS

A negative relationship exists between latitude and all species richness for county-level (r2 = 0.211, p < 0.01) and latitude-band richness (r2 =

0.537, p < 0.01, Table II, Fig. 3). The bimodal pattern in climbing species richness by latitudeband is evident (Fig. 3B). Species richness per band ranges from 48 to 82 in the southern six county bands, but falls at 43.5°N to 30 species and remains < 38 species northward to 44.5°N. Total richness then increases to 44, 39, and 43 species in the three northern bands (45.1, 45.5, and 46.14°N). We evaluated the residuals of all linear regressions (native, non-native, all species, invasive), finding a nonrandom pattern: positive residuals at both low and high latitudes, and negative residuals at mid-latitudes (Fig. 4A shows linear residuals for native species). A quadratic linear model for all four species groups produces both a better fit to the data (Fig. 3B, Table II) and a random pattern of residuals (Fig. 4B shows quadratic residuals for native species). The substantial richness decline at middle latitudes creates a U-shaped pattern of species richness, rather than a linear relationship. SEXUAL SYSTEMS OF MICHIGAN CLIMBERS

Native and non-native species are 65% and 77% hermaphrodites, respectively. Non-natives are no more likely to be hermaphrodites than natives (ztest, p = 0.17384). Among the invasive species (n = 10), 90% are hermaphrodites, not significantly different from native species (z-test, p = 0.114). Michigan’s climbing flora includes 17 dioecious species (16.5%). Among natives, 14 (27%) are dioecious or functionally dioecious, and 3 (6%) are monoecious. In contrast, non-natives include three

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FIG. 5. Distribution of dispersal mode and dispersal unit for 103 climber species in Michigan.

FIG. 4. Residuals of regressions of native species richness over latitude. A. Linear. B. Quadratic

dioecious species (6%) and eight monoecious species (15%, all exotic, see Appendix). Natives and nonnatives are significantly different in dioecy proportions (z-test, p = 0.003), but not significantly different in their monoecy proportions (z-test, p = 0.119). CLIMBER DISPERSAL AGENTS AND DISPERSAL UNITS

Climbing species in Michigan are more often abiotically dispersed than biotically dispersed: 62% vs. 38%, respectively (Fig. 5). Native species are 63% abiotically and 37% biotically dispersed, while non-native species are 62% abiotic, 38% biotic. The ten invasive species are evenly split, with 50% abiotic and 50% biotic dispersal. Based on statewide species lists, abiotic dispersal is predominant. In contrast, biotically dispersed species are more broadly distributed among Michigan counties than abiotic species: 24 of the 41 biotically dispersed species (59%) occur in > 10 counties, while 28 of 61 abiotically dispersed species (46%) occur in > 10 counties. Each biotically dispersed species occurs, on average, in 24.4 counties (range: 1 to 73), whereas abiotically dispersed species occur, on average, in 17.9 counties (range: 1 to 76), however this difference is not significant (z = 1.25, p =

0.2113). The 18 most common native species (present in > 40 counties, Table III) are 61% biotically dispersed. At the latitude scale, each biotically dispersed species occurs on average in 6.6 (s.d. = 4.6) latitude bands, while abiotically dispersed species are present in 5.9 (s.d. = 4.4) bands, a nonsignificant difference (t-test, p > 0.05, Fig. 6). No relationship was found between latitude and dispersal mechanism of climbing species: biotic dispersal varies between 42% and 58% by latitudinal band, with no latitudinal trend (data not shown). Native climbers include 42 to 58% biotically dispersed species per latitude band (10 to 19 species), significantly more than non-native biotically dispersed species (t-test, p < 0.001), which range from 24 to 54% (2 to 12 species) per latitude band (Fig. 6). The dispersal units (fruit vs. seed) of native and non-native species are also significantly different: fruits are more often the dispersal unit of native species (52%), whereas seeds are more common among non-native species (63%; chi-square, p = 0.022; Fig. 5, Appendix). Across all climbing species the dispersal unit is more often a seed than a fruit: 57 versus 45 species, respectively (excluding Lygodium spores). WOODY CLIMBER DISPERSAL COMPARED WITH TREE DISPERSAL

Sixteen species of Michigan native climbers produce woody stems or a woody caudex. Thirteen of these native species (81%) are biotically dispersed. Of the 16 woody species, 11 are found in > 25 of the 83 Michigan counties, including 10 biotically dispersed species (91%) and only a single wind dispersed species: Clematis virginiana L. All four of the

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TABLE III The 18 MOST COMMON NATIVE CLIMBER SPECIES IN MICHIGAN, FOUND IN MORE THAN 40 COUNTIES. COUNTY FREQUENCY, DISPERSAL MODE (ABIOTIC, A; BIOTIC B), AND FRUIT TYPE.

Species Clematis virginiana L. Lonicera dioica L. Vitis riparia Michx. Galium asprellum Michx. Echinocystis lobata (Michx.) Torr. & A. Gray Lathyrus palustris L. Celastrus scandens L. Calystegia sepium (L.) R. Br. Smilax hispida Raf. Amphicarpaea bracteata (L.) Fernald Parthenocissus vitacea (Knerr) Hitchc. Lathyrus ochroleucus Hook. Toxicodendron radicans (L.) Kuntze Menispermum canadense L. Parthenocissus quinquefolia (L.) Planch. Fallopia cilinodis (Michx.) Holub Vicia americana Muhl. Apios americana Medikus

Number of Counties

Dispersal

72 72 65 61 57 57 57 56 55 52 48 46 46 45 44 44 44 41

A B B B B A B A B A B A B B B A A A

woody invasive climbing species are biotically (likely bird) dispersed. Only one exotic woody species is relatively common, Campsis radicans (L.) Bureau, and is wind dispersed and found in 17 counties. While we found no difference in the proportion of native and non-native species dispersed by biotic versus abiotic means, our data demonstrates that biotic dispersal is correlated with woody habit among climbing species. All woody climbers are 76% biotically dispersed. These 34 native, exotic, and invasive woody climbers include 81%, 64%, and 100% biotically dispersed species, respectively. The USDA lists 73 tree species in Michigan, of which 33 (44%) are biotically dispersed and 40 (56%) are abiotically dispersed. Of the 73 tree species, 40 occur in at least 40 counties, and of those, 15 species are biotically dispersed while 25 are abiotically dispersed (37.5% and 62.5%, respectively). Similarly, of the 40 most abundant tree species in Michigan (ranked by the USDA Landscape Change Research Group 2014), 12 (30%) are biotically dispersed and 28 (70%) are abiotically dispersed. Both ranking approaches demonstrate that trees have an opposite dispersal pattern to that of woody climbers; the difference between trees and climbers is significant (chi-square, p < 0.01). For the entire eastern USA, the USDA ranks 25 tree species as most abundant, of which 11 are biotically dispersed and 14 are abiotically dispersed (44 and 56%, respectively). Canham and Thomas (2010) cite 24 tree

Fruit Type plumed achene berry berry hooked schizocarpic nutlets berry (pepo) legume capsule with arillate seeds capsule berry legume berry legume drupe drupe berry achene legume legume

species as the most frequent in eastern North America, including 8 biotically and 16 abiotically dispersed species (33% and 67% respectively).

WOODY VS. HERBACEOUS HABIT AND LIFE SPAN

Michigan climbers are represented by 33% woody species and 67% herbaceous species. The proportion of natives, non-natives, and invasive species are similar, showing no significant differences (Appendix). However, the woody/herbaceous dichotomy obscures the lifespan of individuals because of perennating underground organs, so we

FIG. 6. Native and non-native species differ significantly in their proportion of biotically dispersed species at the latitudeband scale. Natives are much more likely to be dispersed by an animal than are non-native species. Each latitude band is represented by a series of three different symbols in a vertical row.

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also scored species for life span as annual, biennial, or perennial. Among Michigan climbers, one biennial species is known: the relatively uncommon native Adlumia fungosa (Aiton) Greene ex Britton, Sterns, & Poggenb. (Papaveraceae). Native Michigan climbers with underground overwintering organs include Dioscorea villosa L., Apios americana Medik., Ipomoea pandurata (L.) G. Mey., and species of Calystegia R. Br. Of the 51 native species, 10 are annual (20%), and 40 (78%) are perennial (Appendix). The 52 non-native species include 20 annual and 32 perennial species, respectively (38% and 62%). Natives and non-natives lifespans are different, but marginally so (z = 2.05, p = 0.04). Within non-native species, 8 of the 10 invasive climbers are perennial (80%) compared with 24 of 42 (57%) perennial exotic species.

CLIMBING MECHANISMS

Apical twining is the climbing mechanism present most frequently in native species of Michigan (41%, 24 of 51 species, Fig. 7). Examples are Dioscorea villosa, Lonicera dioica L. and L. hirsuta Eaton, two species of Calystegia, and seven species of Cuscuta L. All other mechanisms are represented by nine or fewer species. Petiole tendrils are found in nine native species: five species of Smilax, two species of Clematis, Adlumia fungosa, and Lygodium palmatum. Axillary tendrils and modified-leaflet tendrils are found in seven and six species, respectively. Thus native species include nearly equal proportions of

FIG. 7. Distribution of climbing mechanism among climber species in Michigan. Distribution of species among mechanism type is significantly different between natives and non-natives.

petiole, axillary, and leaflet tendrils (18%, 14%, 12%, respectively). The native climbers of Michigan include only seven species with axillary tendrils, notably four species of Vitis L. Non-native climbing species also are predominantly apically twining, with 60% of invasive species and 38% of exotics using this mechanism. However, the second most common climbing mechanism for both invasive and exotic species is leaf tendrils (30 and 29% of species, respectively), found in many introduced herbaceous legumes such as Lathyrus L. spp. and Vicia L. spp. Among exotic species, a common mechanism is axillary tendrils (21%), mostly represented by species of Cucurbita L., Cucumis L., and Citrullus Schrad. (Cucurbitaceae), whereas none of the invasive species bear axillary tendrils. Climbing mechanisms are significantly different between native and non-native species (chisquare, p = 0.0002). Although they are similar in proportions of apical twiners (47% and 42%, respectively), the high proportion of petiole tendrils in natives, versus high proportions of leaf tendrils in non-native species creates a significant difference in climbing mechanisms. Invasive species are most similar to exotic species, with 30% bearing modified-leaflet tendrils. Discussion SPECIES RICHNESS OF CLIMBERS ACROSS 6° OF LATITUDE IN MICHIGAN

Latitude is correlated with county-level species richness of native climbers in Michigan, while non-native and invasive species are weakly correlated with latitude (Fig. 3). Because a midlatitude decline in species richness is evident across climbers, a quadratic linear regression best fits the decline and rebound over latitude. County species richness is especially high in southern Michigan in Washtenaw county (61 species) and lowest in Gladwin County at 43.5°N latitude (4 species: 2 native and 2 invasive). The bimodal pattern of climber richness was an unanticipated pattern, both the low mid-latitude richness and high richness north of 44.5°N. The pattern may have several contributing causes. First, large areas of federal and state protected land (managed by Department of Natural Resources, DNR) are present north of 44.5°N. There, the amount of preserved land is four times as large as that south of 44.5°N, as reported by Michigan DNR (https:// www.michigan.gov/dnr for PA-240). In fact, ca.

BRITTONIA

700,000 acres are actively managed by the state DNR in the southern half of the state, while > 3,800,000 acres are managed north of 44.5°N. It is perhaps surprising then, that we can find as many native climber species in the south as we do, in an area where development and farmland have replaced native habitats. However, climbing species are often light-loving, and thrive in anthropogenic landscapes, longer growing seasons, and warmer temperatures. Alternatively, the bimodal pattern of species richness over latitude in Michigan may be caused by spatially concentrated work of naturalists, whose botanical collections are part of university or fieldstation based research focused on preserved areas. The southern portion of the state has seven herbaria with > 10,000 specimens each (Thiers, 2015). These herbaria document the intense research activity in surrounding areas (University of Michigan, Michigan State University, Kellogg Biological Station, Cranbrook Institute of Science, Eastern Michigan University, Albion College, and Andrews University). In contrast, the central portion of the state has substantially fewer herbaria (only Central Michigan University and Alma College have over 10,000 specimens), while northern Michigan includes two large universities (Michigan Technological University and Northern Michigan University), the Huron Mountain Foundation Research Center, Isle Royal National Park, and the University of Michigan Biological Station, which is a hub for local collections and has its own 18,000+ specimen herbarium. A third factor that may affect climbing species distribution is human population distribution and second home distribution. Both distributions show a weakly bimodal pattern (Fig. 1), comparable to all climbers. In the upper peninsula of Michigan four counties include six invasive species each: 60% of the invasive climbers in the state. These are Schoolcraft, Keewenaw, Ontonagon, and Marquette counties, including three of the four largest counties in the state. However, only Marquette county has a population > 50,000, the rest have < 10,000, according to the 2010 population census (http://www.census.gov/2010census/data/). However, Keewenaw county, with a small size and low population density has one of the highest proportions of second homes in the United States (http://www.census.gov/2010census/data/). This suggests that humans influence the high nonnative richness in various ways: vacation and permanent population density, intense collecting activity, and large tracts of recreational land. Finally, climate may contribute to the bimodal pattern.

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Two upper peninsula counties with > 20 native species are Menominee and Ontonogon. The first experiences areas of longer growing season than most counties in the upper peninsula and includes mild lakeshore habitat (Lake Michigan). Ontonogon county, with 22 native species, is the third largest county in the state, has an extensive milder lakeshore (Lake Superior), and includes both long and short growing season areas. The diversity drop at mid-latitudes may reflect fewer active research centers, fewer large preserved areas, lower numbers of vacation homes, but a distinctly short growing season may be the ultimate reason. While the upper peninsula experiences areas with short growing seasons, short growing seasons are also documented in the northern half of the lower peninsula in a northeast to southwest orientation (Eichenlaub et al., 1990). Growing season length of only 90 days are documented at Gaylord, Michigan (Ostego county), equivalent to the shortest known growing seasons in the upper peninsula (National Weather Service: http:// www.weather.gov/apx/climatology_frost). At midlatitudes, the low species richness counties in the interior of the state are bordered by lakeside counties with higher richness along the Great Lakes (e.g., Manistee, Benzie, Leelenaw). In the southern portion of Michigan, preservation in national, county, and state parks, more moderate winters, longer and warmer summers, and a rich history of naturalists making plant collections contributes to a record of high climber richness (Fig. 2A, C). Washtenaw and Kalamazoo counties, at 42.2°N, are home to three of the major universities in Michigan, include large tracts of preserved land managed by the state DNR, universities, or county authorities and have growing season lengths of about 170 days. These two counties include the second and third largest number of native climbers (35 and 37, respectively), and Washtenaw has the largest number of non-native species (26). During our research we noted an anomalously low number of species in Branch county (n = 16) at 41.5°N latitude. We then made two single-day collecting trips to Branch county natural areas near Union City and Coldwater, collecting 13 new records for the county, and bringing the total richness for Branch county into line with other counties at this latitude (band average = 39 species, s.d.= 9.8). The new collections for this county are included here. In spite of the wealth of material in various herbaria of the state, there are still gaps in climbing species

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distributions. Both Eaton and Shiawassee counties in southern Michigan show low total abundance of climbers (Fig. 2A), and may represent instances of under-collection. This experience suggests caution in over-interpreting the climate explanation until the mid-latitudes receive similar attention. SEXUAL SYSTEMS OF MICHIGAN CLIMBERS

Baker’s Law (1955, 1974) proposes that colonizing species are most likely to be uniparental (monoecious or hermaphroditic). This applies to woody invasive plants in South Africa (Rambuda & Johnson, 2004) and to colonizing vines on Krakatau (Bush et al., 1995). We predicted that non-native climbing species in Michigan also include more uniparental species than do natives. Native and non-native climbers are not statistically different in proportion of hermaphrodites in Michigan, contrary to our hypothesis, yet we suggest that hermaphroditic exotic climbers should be closely monitored (31 species, Appendix), as they have a greater potential for becoming invasive. As predicted, dioecious species are more common among natives than non-natives, and monoecy is less common (however, non-significantly) among natives than among non-natives. Similar differences were found for invasive species elsewhere (Baker, 1955, 1967; Rambuda & Johnson, 2004; Herron et al., 2007), but dioecy proportions of 24% have been documented among colonizing vines (Bush et al., 1995). None of the invasive vine species in Michigan are known to be monoecious. Eight monoecious species are included among non-natives (all exotic: six Cucurbitaceae, one Lardizabalaceae, one Sapindaceae), whereas only two dioecious species (one Cucurbitaceae and one Cannabaceae) are exotics. Theory predicts that the eight monoecious species are more likely to become invasive than the two dioecious species, however sexual system is but one trait affecting species’ distribution. Celastrus orbiculatus Thunb., an aggressive functionally dioecious invader (Ladwig & Meiners 2010b), clearly indicates that a single trait is not reliable in predicting invasive status. Important traits often found in invasive climbers include abundant resprouting, bird dispersal, historical residence time, and climatic range (Hayes & Barry, 2008; Ahern et al., 2010). Renner (2014) documented 5–6% of all angiosperms as dioecious, concentrated in 34 clades of exclusively dioecious species. This value is lower than the maximum value suggested by Bawa (1980) for regional floras (25%), however Bawa’s concept

of dioecy included a broader range of sexual systems. Bawa reported 3.5% dioecy in the flora of North Carolina, but noted that 16% of the climbing species there were dioecious. Considering tropical sites, Gentry (1991b) reported 10% dioecy among climbers of Barro Colorado Island, Panama and the same proportion in Chamela, Mexico. In the tropical flora of Tambopata, Peru, Vamosi et al. (2008) cite 16% dioecy among woody climbers. Michigan’s current flora includes 16.5% dioecious climbers and 27% dioecious native climbers. At least three scenarios may explain our finding of high dioecy: 1) the climbing habit is phylogenetically constrained, potentially limiting sexual systems as well, 2) climbing species are exposed to selective filters distinct from those of other growth forms, or 3) a link between dioecy and biotic dispersal (Vamosi et al., 2007) may give these species an advantage and operates in temperate climbers. DISPERSAL SYNDROMES

Thompson et al. (1995) found no correlation between wind-dispersed diaspores and Balien^ frequency in western Europe, whereas a global survey by Richardson and Rejmánek (2011) found that invasive tree and shrub species are most often dispersed by birds. Both studies agree with dispersal patterns of climbers in Michigan. In contrast, the colonizing climber species of Krakatau, Indonesia include twice as many abiotically dispersed (sea and wind) as biotically dispersed species (Bush et al., 1995). Dispersal mode is often phylogenetically linked (Lord et al., 1995; Gallagher & Leishman, 2012), and of 39 biotically dispersed climbers in Michigan, 27 are found in just four families: Cucurbitaceae, Vitaceae, Caprifoliaceae, and Smilacaceae. Similarly, the majority of climbers in the Fabaceae (29 of 30) are abiotically dispersed via ballistics or gravity. Success in the relatively harsh winters of Michigan may depend more on xylem and phloem innovations that allow species to overwinter, than it does on dispersal mechanism. Non-native climbers include several species bearing large fruits that are not easily dispersed intact by the non-human mammals of Michigan today, especially in the Cucurbitaceae. Combined with the 19 non-native seed-dispersed Fabaceae species likely escaped from cultivation, this produces a high proportion of seeds acting as dispersal units among non-natives (Fig. 5).

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BRITTONIA DISPERSAL IN WOODY CLIMBERS AND TREES

CLIMBING MECHANISMS

In Neotropical floras, lianas are more often wind-dispersed than are trees (Gentry, 1982, 1983, 1991b; Wright et al., 2007). There, the proportion of wind dispersed climber species is frequently about 50% (Gentry, 1991b; Solórzano et al., 2002; Gallagher & Leishman, 2012), and > 70% in dry forests (Gentry, 1991b; Gillespie, 1999). Michigan climbers collectively include 62% abiotically dispersed species, many of which are gravity or water dispersed, lacking any wing or plume for wind dispersal (Fig. 5). However, few native climbing species are wind dispersed in Michigan: Mikania scandens (L.) Willdenow, Clematis virginiana, and Dioscorea villosa are the only obviously winged diaspores among natives. This is counter to Neotropical observations (Gentry 1983, 1991b), but even Gentry noted (1991b) that samples from temperate regions (all woody species) included only bird-dispersed climbers. He also noted that only one-third of the climbers in the southeastern U.S. flora were wind dispersed (data from Duncan, 1975). Ladwig and Meiners (2010b) work on succession in New Jersey report five species of climbers that are most abundant, all of which are animal (probably bird) dispersed. Common trees in Michigan are more often wind dispersed than animal dispersed (Gentry 1991b, our data), and more often wind dispersed than common woody climbers. High species diversity within wind-dispersed tree genera like Ulmus L., Fraxinus L., Acer L., Betula L., Alnus Mill., Populus L. contribute to this pattern. Data from Indiana and Ohio (Howe & Smallwood, 1982) also show a higher proportion of wind than animal dispersal in tree species, contrary to tree dispersal in the tropics.

Similar to floras worldwide (Muthuramkumar & Parthasarathy, 2001; Burnham & RevillaMinaya, 2011; Gallagher & Leishman, 2012; Durigon et al., 2014), apical twining is the predominant climbing mechanism of Michigan climbers (Fig. 7). Non-native species bearing tendrils in Michigan differ from natives in the organs modified for grasping host supports (leaflets versus petioles). Although the grape industry may characterize Bvines^ as plants bearing axillary tendrils, that climbing mechanism is less common worldwide than apical twining (DeWalt et al., 2000; Chittibabu & Parthasarathy, 2001; Addo-Fordjour et al., 2013). Even invasive species in Michigan are 60% apical twiners.

WOODY HABIT AND LIFE SPAN

Abundant perennial species among native (78%), invasive (80%), and exotic (57%) climbers suggests that the relatively short growing season in the Upper Midwest of the United States is a selective deterrent to species whose primary means of spread is by annual seed production. Our prediction of abundant herbaceous perennials and annuals among exotic species was supported, but annuals are uncommon among climbing invasive species. We predict that perennial species have the greatest potential to transition from benign exotics to invasive threats.

PREDICTED FUTURE INVASIVE CLIMBERS IN MICHIGAN

Several exotic climbing species are expanding their range in areas beyond Michigan, and may spread dramatically under increased disturbance, seasonal change, temperature, or increased CO2 (see review in Harris & Gallagher, 2010). Aggressive climbing species that are common in states near Michigan include Ampelopsis brevipedunculata (Maxim.) Trautv., Clematis terniflora DC., Euonymus fortunei (Turcz.) Hand.Mazz., Hedera helix, Persicaria perfoliata (L.) H. Gross, Pueraria montana (Lour.) Merr., Vicia cracca L., V. sativa L., Vincetoxicum rossicum (Kleopov.) Barbar., and Wisteria sinensis (Sims) DC., any of which we propose are potential invasives in Michigan. Most of these species are perennial and hermaphroditic, and more than half are abiotically dispersed with organs specially modified as climbing mechanisms. These characteristics are those most likely to transform exotic species into invasives in Michigan. Two currently invasive species in Michigan, properly classified as scramblers, not climbers, are Securigera varia (L.) Lassen (Fabaceae) and Vinca minor L. (Apocynaceae). Conclusions We found that species richness of climbers is only weakly correlated with latitude, instead showing a strong mid-latitude decline, likely due to several factors including short growing seasons. We confirmed that more dioecious species are among the native species than non-natives, but that monoecy is no more common among natives than non-natives. Contrary to our hypothesis, we found

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that dispersal modes are equivalent among the three classes of climbers, however woody climbers are significantly more animal dispersed than are herbaceous climbers. Annual climbers are rare among native species, but comprise almost half of exotic species. Short growing seasons over much of Michigan likely prevent many annuals from completing their life cycle prior to killing frosts. A substantial number of invasive species are woody and perennial, characteristics that predispose them to success in Michigan climates. As anticipated, twining mechanisms are broadly similar among climber classes, with variations in tendril position linked to phylogenetic group. The 103 climbing species currently found in Michigan form a single frame of a moving picture. Arrival of new climbing species from garden introductions and northward migration is expected under increasing global temperatures. The present climbing flora is almost evenly split between native and non-native species. Ahern et al. (2010) documented 34% non-native species in Michigan, including all life forms, which suggests that climbers are more often introduced than other life forms. The good news, that only ten non-native species currently are broadly invasive, is tempered by the speed and distance over which these ten species have spread (Appendix). The non-native species include many legumes (Fabaceae), often used as cover crops or existing as weeds in agricultural fields and roadsides. Prior research on woody climbers (Tibbetts & Ewers, 2000) suggested that climbers contribute 1% of the Michigan flora (29 of 2465 species), but in including both herbaceous and exotic species, as we have here, the contribution is closer to 4% of angiosperms. Herron et al. (2007) suggested that an Bopen niche^ was available to climbers in temperate forests, even though substantial diversity of climbers exists now. The high number of exotic species does suggest that additional species can be accommodated in temperate forests without displacing natives. Surprisingly little research has been published on the relative frequency of climbers over time in northern temperate forests. Pre-colonial ecosystem diversity of Michigan was enriched by native species that provided animal populations with fleshy fruits: wild grapes (Vitis spp.), native bittersweet (Celastrus scandens L.), Virginia creeper (Parthenocissus spp.), and native honeysuckle (Lonicera spp.). Climber species contribute to fruit diversity, extend the period of available fruits, and add fruits at different sites and heights than shrubs and trees. Non-native

climbers also add to biodiversity, yet the invasive species among them are substantial threats because of widespread and rapid expansion. This study adds to an emerging literature on temperate climbers, which have been poorly studied. Our aim, in documenting the relatively high species richness of climbers in Michigan is to stimulate comparative research on climbing species in other temperate areas.

Acknowledgements The authors are grateful to numerous undergraduate botanists, too many to be named here, who assisted with database compilation for Michigan Climbers. In particular we appreciate the dedication of Marko Melymuka and ReBecca Sonday in the early database stages, and Claire Malley for website design and construction. We also appreciate the support of Nicole Scholtz (U of M Clark Map Library) for advice on mapping. We thank two anonymous reviewers for very helpful commentary which substantially improved the manuscript. The research was supported in part by a grant to RJB from the University of Michigan School of Literature, Science, and the Arts. Literature Cited Addo-Fordjour, P., P. El Duah & D.K.K. Agbesi. 2013. Factors influencing liana species richness and structure following anthropogenic disturbance in a tropical forest, Ghana. International Scholarly Research Notices Forestry 2013, Article ID 920370, 11 pages. Ahern, R. G., D. A. Landis, A. A. Reznicek & D. W. Schemske. 2010. Spread of exotic plants in the landscape: the growth habit and history of invasiveness. Biological Invasions 12: 3157–3169. Austin, D. F. 2000. Bindweed (Convolvulus arvensis, Convolvulaceae) in North America, from medicine to menace. Journal of the Torrey Botanical Society 127(2): 172–177. Baker, H. G. 1955. Self-compatibility and establishment after ‘long-distance’ dispersal. Evolution 9(3): 347–349. ———. 1967. Support for Baker's law — as a rule. Evolution 21(4): 853–856. ———. 1974. The evolution of weeds. Annual Review of Ecology and Systematics 5: 1–24. Banasiak S. E. & S. J. Meiners. 2009. Long term dynamics of Rosa multiflora in a successional system. Biological Invasions 11: 215–224. Barnes, B. V. & W. H. Wagner. 1992. Michigan Trees: A guide to the trees of Michigan and the Great Lakes Region. The University of Michigan Press, Ann Arbor. Bawa, K. 1980. Evolution of dioecy in flowering plants. Annual Review of Ecology and Systematics 11: 15–39. Billington, C. 1943. Shrubs of Michigan. Cranbrook Institute of Science, Bloomfield Hills.

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———. 2010b. Liana host preference and implications for deciduous forest regeneration. Journal of the Torrey Botanical Society 137(1): 103–112. Landscape Change Research Group. 2014. Climate change atlas. Northern Research Station, U.S. Forest Service, Delaware, OH. http://www.nrs.fs.fed.us/atlas. Lanini, W. T. & M. Kogan. 2005. Biology and management of Cuscuta in Crops. Ciencia E Investigacion Agraria 32(3): 127–141. Leicht-Young, S. A., N. B. Pavlovic, K. J. Frohnapple & R. Grundel. 2010. Liana habitat and host preferences in northern temperate forests. Forest Ecology and Management 260(9): 1467–1477. Lord, J., M. Westoby & M. Leishman. 1995. Seed size and phylogeny in six temperate floras: constraints, niche conservatism, and adaptation. The American Naturalist 146(3): 349–364. Lutz, H. J. 1943. Injuries to trees caused by Celastrus and Vitis. Bulletin of the Torrey Botanical Club 70(4): 436–439. Madden, M., R. Welch, T. Jordan, P. Jackson, R. Seavey & J. Seavey. 2004. Digital vegetation maps for the Great Smokey Mountains National Park. Final Report submitted to U.S. Department of Interior National Park Service. http://www1.usgs.gov/vip/grsm/grsmrpt.pdf Michigan Flora Online. A. A. Reznicek, E. G. Voss & B. S. Walters. February 2011 and onwards. University of Michigan. http://michiganflora.net/home.aspx. Miller, J. H., E. B. Chambliss & N. J. Loewenstein. 2010. Field guide for the identification of invasive plants in southern forests. Asheville, NC: U.S.D.A. Forest Service Southern Research Station. General Technical Report SRS-119. Molano-Flores, B. 2014. An invasive plant species decreases native plant reproductive success. Natural Areas Journal 34(4): 465–469. Muthuramkumar, S. & N. Parthasarathy. 2001. Alpha diversity of lianas in a tropical evergreen forest in the Anamalais, Western Ghats, India. Diversity and Distributions 6(1): 1–14. Parker, G. R. & G. Schneider. 1975. Biomass and productivity of an alder swamp in northern Michigan. Canadian Journal of Forest Research 5(3): 403–409. Patterson, D. T. 1976. The history and distribution of five exotic weeds in North Carolina. Castanea 41: 177–180. Pavlovic, N. B. & S. A. Leicht-Young. 2011. Are temperate mature forests buffered from invasive lianas? Journal of the Torrey Botanical Society 138(1): 85–92. Pérez-Salicrup, D. R. 2001. Effect of liana cutting on tree regeneration in a liana forest in Amazonian Bolivia. Ecology 82(2): 389–396. Rambuda, T. D. & S. D. Johnson. 2004. Breeding systems of invasive alien plants in South Africa: does Baker's rule apply? Diversity and Distributions 10(5-6): 409–416. Renner, S. 2014. The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. American Journal of Botany 101(10): 1588–1596. Richardson, D. M. & M. Rejmánek. 2011. Trees and shrubs as invasive alien species – a global review. Diversity and Distributions 17(5): 788–809. Royer, F. & R. Dickinson. 1999. Weeds of the northern U.S. and Canada. University of Alberta Press, Edmonton. Schnitzer, S. A. 2005. A mechanistic explanation for global patterns of liana abundance and distribution. The American Naturalist 166: 262–276

——— & F. Bongers. 2002. The ecology of lianas and their role in forests. Trends in Ecology and Evolution 17(5): 223–230. Siccama, T. G., G. Weir & K. Wallace. 1976. Ice damage in a mixed hardwood forest in Connecticut in relation to Vitis infestation. Bulletin of the Torrey Botanical Club 103: 180–183. Solórzano, S., G. Ibarra-Manríquez & K. Oyama. 2002. Liana diversity and reproductive attributes in two tropical forests in Mexico. Biodiversity and Conservation 11: 197–212. Stone, K. R. 2009. Cynanchum louiseae, C. rossicum. In: Fire Effects Information System, [Online]. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fire Sciences Laboratory. http://www.fs.fed.us/database/feis/ Thiers, B. 2015. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden's Virtual Herbarium. http://sweetgum.nybg.org/ih/ Thompson, K., J. G. Hodgson & T. C. G. Rich. 1995. Native and alien invasive plants: more of the same? Ecography 18(4): 390–402. Tibbetts, T. J. & F. W. Ewers. 2000. Root pressure and specific conductivity in temperate lianas: exotic Celastrus orbiculatus (Celastraceae) vs. native Vitis riparia (Vitaceae). American Journal of Botany 87(9): 1272–1278. Vamosi, S. M., S. J. Mazer, & F. Cornejo. 2008. Breeding systems and seed size in a Neotropical flora: testing evolutionary hypotheses. Ecology 89(9): 2461–2472. Vamosi, J. C., Y. Zhang, & W. G. Wilson. 2007. Animal dispersal dynamics promoting dioecy over hermaphroditism. The American Naturalist 170(3): 485–491. Voss, E. G. 1972. Michigan Flora Part I: Gymnosperms and Monocots. Cranbrook Institute of Science, Ann Arbor. ———. 1985. Michigan Flora Part II: Dicots. Cranbrook Institute of Science, Ann Arbor. ———. 2004. Michigan Flora Part III: Dicots Concluded. Cranbrook Institute of Science, Ann Arbor. ——— & A. Reznicek. 2012. Field manual of Michigan flora. University of Michigan Press, Ann Arbor. Waggy, M. A. 2009. Solanum dulcamara. In: Fire Effects Information System, [Online]. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fire Sciences Laboratory. Available: http://www.fs.fed.us/ database/feis/ Welch, R. W. 1972. County evolution in Michigan 1790 – 1897. Michigan Department of Education State Library Services Occasional Paper No 2, Lansing, MI. Wells, J. R. & P. W. Thompson. 1972. Field key to some common shrubs and vines of Michigan. The Michigan Botanist 11: 129–139. Wright, S. J., A. Hernandéz & R. Condit. 2007. The bushmeat harvest alters seedling banks by favoring lianas, large seeds, and seeds dispersed by bats, birds, and wind. Biotropica 39(3): 363–371. Yanoviak, S. P. 2013. Shock value: are lianas natural lightning rods? Pp. 147–153 In: M. Lowman, S. Devy & T. Ganesh (eds.). Treetops at Risk: Challenges of Global Forest Canopies. Springer, New York, NY. Zaroug, M. S., E. A. B. Zahran, A. A. Abbasher & E. A. A. Aliem. 2014. Host range of field dodder (Cuscuta campestris Yuncker) and its impact on onion (Allium cepa L.) cultivars grown in Gezira state Sudan. International Journal of AgriScience 4(7): 356–361. Zuloaga, F. O., O. N. Morrone, M. J. Belgrano, C. Marticorena & E. Marchesi (eds.). 2008. Catálogo de las plantas vasculares del Cono Sur. Monographs Systematic Botany Missouri Botanical Garden 107: 1–3348.

Native in Michigan Adlumia fungosa (Aiton) Greene ex Britton, Sterns & Poggenb. Amphicarpaea bracteata (L.) Fernald Apios americana Medik. Calystegia sepium (L.) R. Br. Calystegia silvatica (Kit.) Griseb. Celastrus scandens L. Clematis occidentalis (Hornem.) DC Clematis virginiana L. Cuscuta cephalanthi Engelm. Cuscuta coryli Engelm. Cuscuta glomerata Choisy Cuscuta gronovii Willd. ex Schultes Cuscuta indecora Choisy Cuscuta pentagona Engelmann Cuscuta polygonorum Engelmann Dioscorea villosa L. Echinocystis lobata (Michaux) Torr. & Gray. Fallopia scandens (L.) Holub Fallopia cilinodis (Michx.) Holub Galium asprellum Michx. Humulus lupulus L. Ipomoea pandurata (L.) G. Mey. Lathyrus japonicus Willd. Lathyrus ochroleucus Hook. Lathyrus palustris L. Lathyrus venosus Muhl. ex Willd. Lonicera dioica L. Lonicera hirsuta Eat. Lygodium palmatum (Bernh.) Swartz Menispermum canadense L.

Latin Name and Authority Papaveraceae Fabaceae Fabaceae Convolvulaceae Convolvulaceae Celastraceae Ranunculaceae Ranunculaceae Convolvulaceae Convolvulaceae Convolvulaceae Convolvulaceae Convolvulaceae Convolvulaceae Convolvulaceae Dioscoreaceae Cucurbitaceae Polygonaceae Polygonaceae Rubiaceae Cannabaceae Convolvulaceae Fabaceae Fabaceae Fabaceae Fabaceae Caprifoliaceae Caprifoliaceae Schizaeaceae Menispermaceae

Family HB HP HP HP HP WP WP WP HA HA HA HP HP HA HA HP HA HP HP HP HP HP HP HP HP HP WP WP HP WP

Life Habit P P P P P D P D P P P P P P P D M P P P D P P P P P P P O D

Sexual System A (self-sown) A (ballistic) A (dehiscent) A (gravity, water) A (gravity, water) B (bird) A (plumed) A (plumed) A (gravity) A (gravity) A (gravity) A (gravity) A (gravity) A (gravity) A (gravity) A (winged) B (ballistic, animal) A (wind) or B (bird) A wind(?) B (bird / exochory) A (wind) A (wind, gravity) A (water) [B? bird] A (gravity) A (gravity) A (gravity) B (bird, mammal) B (bird, mammal) A (wind) B (bird)

Dispersal Mechanism

seed seed seed seed seed seed achene achene seed seed seed seed seed seed seed seed, fruit seed achene achene achene achene seed seed seed seed seed fruit fruit spore fruit

Dispersal Unit

Petiole Apical Apical Apical Apical Apical Petiole Petiole Apical Apical Apical Apical Apical Apical Apical Apical Axillary Apical Apical Spine, Hook Apical Apical Leaflet Leaflet Leaflet Leaflet Apical Apical Petiole Apical

Climbing Mechanism

TABLE IV CLIMBING SPECIES OF Michigan, LISTED ALPHABETICALLY BY GENUS WITHIN THE THREE MAJOR GROUPS ANALYZED: NATIVE, INVASIVE, AND EXOTIC. ALSO LISTED FOR THE 103 SPECIES ARE LIFE HABIT, INFERRED SEXUAL SYSTEM, DISPERSAL MECHANISM, AND UNIT OF DISPERSAL. LIFE HABITS: W=WOODY, H=HERBACEOUS, P= PERENNIAL, A= ANNUAL, B= BIENNIAL. SEXUAL SYSTEM: P=HERMAPHRODITIC; M= MONOECIOUS; D= DIOECIOUS; O=OTHER. DISPERSAL MECHANISM A= ABIOTIC, B= BIOTIC. DISPERSAL UNIT LISTED AS FRUIT (INCLUDING ACHENE) OR SEED.

Appendix

BRITTONIA

[VOL

Non-native and Invasive in Michigan (date of US introduction) Celastrus orbiculatus Thunb. (1874; Del Tredici, 2014) Convolvulus arvensis L. (1730; Austin, 2000) Fallopia convolvulus (L.) A. Löve (1860; Royer & Dickinson, 1999) Lathyrus latifolius L. (1700sa) Lathyrus sylvestris L. introduction unknown Lonicera japonica Thunb. (pre-1860; Patterson, 1976) Rosa multiflora Thunb. (pre-1811; Patterson, 1976) Solanum dulcamara L. (mid-1800s; Waggy, 2009) Vicia villosa Roth (~1800; Hannaway & Larson, 2004) Vincetoxicum nigrum (L.) Pers. (mid to late-1800s; Stone, 2009)

Mikania scandens (L.) Willdenow Parthenocissus quinquefolia (L.) Planch. Parthenocissus vitacea (Knerr) A. Hitchcock Persicaria arifolia (L.) Haraldson Persicaria sagittata (L.) H. Gross Phaseolus polystachios (L.) Britton, Sterns & Poggenb. Sicyos angulatus L. Smilax herbacea L. Smilax hispida Raf. Smilax illinoensis Mangaly Smilax lasioneura Hooker Smilax rotundifolia L. Strophostyles helvula (L.) Elliot Toxicodendron radicans (L.) Kuntze Vicia americana Muhl. Vicia caroliniana Walter Vitis aestivalis Michaux Vitis labrusca L. Vitis riparia Michx. Vitis vulpina L. Wisteria frutescens (L.) Poir.

Latin Name and Authority

Celastraceae Convolvulaceae Polygonaceae Fabaceae Fabaceae Caprifoliaceae Rosaceae Solanaceae Fabaceae Apocynaceae

Asteraceae Vitaceae Vitaceae Polygonaceae Polygonaceae Fabaceae Cucurbitaceae Smilacaceae Smilacaceae Smilacaceae Smilacaceae Smilacaceae Fabaceae Anacardiaceae Fabaceae Fabaceae Vitaceae Vitaceae Vitaceae Vitaceae Fabaceae

Family

WP HP HA HP HP WP WP WP HA HP

HP WP WP HA HA HP HA HP WP HP HP WP HA WP HP HP WP WP WP WP WP

Life Habit

TABLE IV (CONTINUED).

D P P P P P P P P P

P P P P P P M D D D D D P M P P D D D D P

Sexual System

B (bird, mammal) B (bird) A (gravity, wind) A (gravity, ballistic) A (gravity, ballistic) B (bird, mammal) B (bird, mammal) B (bird, mammal) A (ballistic) A (wind, plumed)

A (wind) B (bird) B (bird) A (gravity) A (gravity) A (ballistic) B (exochorous) B (bird, mammal) B (bird, mammal) B (bird, mammal) B (bird, mammal) B (bird, mammal) A (ballistic) B (bird) A (ballistic) A (ballistic) B (bird, mammal) B (bird, mammal) B (bird, mammal) B (bird, mammal) A (gravity)

Dispersal Mechanism

seed seed achene seed seed seed seed fruit seed seed

achene fruit fruit achene achene seed fruit fruit fruit fruit fruit fruit seed fruit seed seed fruit fruit fruit fruit seed

Dispersal Unit

Apical Apical Apical Leaflet Leaflet Apical Spine, Hook Apical Leaflet Apical

Apical Suction Axillary Spine, Hook Spine, Hook Apical Axillary Petiole Petiole Petiole Petiole Petiole Axillary Root Leaflet Leaflet Axillary Axillary Axillary Axillary Apical

Climbing Mechanism

2015] MICHIGAN CLIMBERS

Exotic in Michigan Akebia quinata (Houtt.) Decne. Ampelopsis aconitifolia Bunge Ampelopsis brevipedunculata (Maxim.) Trautv. Calystegia pubescens Lindl. Campsis radicans (L.) Bureau Cardiospermum halicacabum L. Citrullus lanatus (Thunb.) Matsum. & Nakai Clematis terniflora DC. Cucumis melo L. Cucumis sativus L. Cucurbita foetidissima H. B. Kunth. Cucurbita maxima Duchesne Cucurbita pepo L. Cuscuta epithymum Murray Euonymus fortunei (Turcz.) Handel-Mazz. Hedera helix L. Humulus japonicus Sieb & Zucc. Ipomoea hederacea (L.) Jacq. Ipomoea purpurea (L.) Roth Isotrema macrophyllum (Lam.) C.F. Reed Isotrema tomentosum (Sims) H. Huber Lathyrus hirsutus L. Lathyrus odoratus L. Lathyrus pratensis L. Lathyrus tuberosus L. Lonicera caprifolium L. Lonicera reticulata Raf. Lonicera sempervirens L. Phaseolus vulgaris L. Pisum sativum L. Pueraria montana (Lour.) Merr. Thladiantha dubia Bunge Vicia cracca L.

Latin Name and Authority

Lardizabalaceae Vitaceae Vitaceae Convolvulaceae Bignoniaceae Sapindaceae Cucurbitaceae Ranunculaceae Cucurbitaceae Cucurbitaceae Cucurbitaceae Cucurbitaceae Cucurbitaceae Convolvulaceae Celastraceae Araliaceae Cannabaceae Convolvulaceae Convolvulaceae Aristolochiaceae Aristolochiaceae Fabaceae Fabaceae Fabaceae Fabaceae Caprifoliaceae Caprifoliaceae Caprifoliaceae Fabaceae Fabaceae Fabaceae Cucurbitaceae Fabaceae

Family

TABLE IV (CONTINUED).

WP WP WP HP WP HA HA WP HA HA HP HA HA HP WP WP HA HA HA WP WP HP HA HP HP WP WP WP HA HA HP HP HP

Life Habit

M P O P P M M P M M M M M P P P D P P P P P P P P P P P P P P D P

Sexual System

B (bird, mammal) B (bird, mammal) B (bird, mammal) A (gravity, water) A (wind) A (wind, self-sown) B (bird, mammal) A (plumed) B (bird, mammal) B (bird, mammal) B (bird, mammal) B (bird, mammal, water) B (bird, mammal) A (gravity) B (bird, mammal) B (bird) A (wind, water) A (gravity) A (gravity) A (wind, gravity) A (wind, gravity) A (ballistic) A (ballistic) A (ballistic) A (ballistic) B (bird, mammal) B (bird, mammal) B (bird, mammal) A (ballistic) A (gravity?) B (bird, mammal?) A (unknown for MI) A (ballistic)

Dispersal Mechanism

seed fruit fruit seed seed fruit seed achene seed seed seed seed seed seed seed seed achene seed seed seed seed seed seed seed seed fruit fruit fruit seed seed seed seed? seed

Dispersal Unit

Apical Axillary Axillary Apical Root Axillary Axillary Petiole Axillary Axillary Axillary Axillary Axillary Apical Root Root Apical Apical Apical Apical Apical Leaflet Leaflet Leaflet Leaflet Apical Apical Apical Apical Leaflet Apical Axillary Leaflet

Climbing Mechanism

BRITTONIA

[VOL

Lathyrus latifolius date of introduction reference:

1

HA HA HA HA HP HA HA HP WP

Life Habit P P P P P P P P P

Sexual System A (self-sown) A (ballistic) A (ballistic) A (ballistic) A (ballistic) A (ballistic) A (ballistic) A (wind: plumose) A (ballistic)

Dispersal Mechanism seed seed seed seed seed seed seed seed seed

Dispersal Unit

Leaflet Leaflet Leaflet Leaflet Leaflet Leaflet Apical Apical Apical

Climbing Mechanism

Missouri Botanical Garden Plant Finder: http://www.missouribotanicalgarden.org/PlantFinder/ PlantFinderDetails.aspx?kempercode=d661

Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Apocynaceae Fabaceae

Vicia grandiflora Scop. Vicia hirsuta (L.) Gray Vicia lathyroides L. Vicia sativa L. Vicia sepium L. Vicia tetrasperma (L.) Schreb. Vigna unguiculata (L.) Walp. Vincetoxicum rossicum (Kleopow) Borhidi Wisteria sinensis (Sims) DC.

a

Family

Latin Name and Authority

TABLE IV (CONTINUED).

2015] MICHIGAN CLIMBERS