Morphological Traits of Common Autumn-ripening Bird-dispersed Fruits in Southeastern MichiganSkip other details (including permanent urls, DOI, citation information)
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. Please contact email@example.com to use this work in a way not covered by the license. :
For more information, read Michigan Publishing's access and usage policy.
10 THE GREAT LAKES BOTANIST Vol. 56
MORPHOLOGICAL TRAITS OF COMMON AUTUMN-RIPENING BIRD-DISPERSED FRUITS IN SOUTHEASTERN MICHIGAN
Julie Craves Rouge River Bird Observatory University of Michigan-Dearborn Dearborn, MI 48128 firstname.lastname@example.org
Fruit size, seed load, and seed size are considered important metrics that influence fruit choice and subsequent seed dispersal by birds. I describe these traits for 37 plant taxa in southeastern Michi- gan, based on measurements of over 5,800 fruits and 8,000 seeds. I also provide literature reports of nearly 200 measurements for the same taxa. These data can be used in biogeographical studies and can also aid in conservation and restoration efforts by describing the traits that are preferred by birds, which in turn influence seed dispersal through landscapes.
Seed dispersal mechanisms drive plant population dynamics. In temperate zones, up to half of all plant species may have fleshy fruits (Willson 1986; Will- son et al. 1989; Uriarte et al. 2011), and birds are their primary dispersers (Snow and Snow 1988; Greenberg and Walter 2010). Thus, birds are major agents in the movement of seeds through landscapes and act as important architects of plant demographics (Jordano 2000; Uriarte et al. 2011). Recognition of the traits that increase the probability of fruit selection and the quality of the resulting seed dispersal adds to our understanding of the spread and distribution of bird-dis- persed plants (Gosper et al. 2005; Buckley et al. 2006; Westcott and Fletcher 2011; McConkey et al. 2012).
Fruit choice in birds is a complex, often hierarchial, process (McPherson 1987; Sallabanks 1993; Foster 2008). Potential factors that may influence bird visits to fruiting plants are plant abundance and neighborhood composition (Sar- gent 1990; Carlo 2005), crop size (Denslow 1987; Takahashi and Kamitani 2004; Blendinger and Villegas 2011), plant structure and fruit accessibility (Moermond and Denslow 1983; Levey et al. 1984), and display (Willson and Melampy 1983; Whelan and Willson 1994). Individual fruit selection may be guided by physical fruit traits including color, chemistry, size, seed load, and seed size (Levey 1987; Nakanishi 1996; Gosper et al. 2005; Jordano 2000).
Fruit size is a critical trait, as birds seek to maximize handling eff iciency and are limited by the size of their gapes (Herrera 1984; Wheelwright 1985; Levey 1987; Jordano 2000). Seed size often determines the distance and spatial pat- terns of dispersal (Hernández 2009; Uriarte et al. 2011). Large seeds (relative to
Page 11 2017 THE GREAT LAKES BOTANIST 11
bird size) are usually dropped or regurgitated close to the parent plant, whereas small seeds are typically swallowed and later defecated, often some distance away; a longer gut retention time in the latter case may also enhance germination (Johnson et al. 1985; Levey 1987; Hoppes 1988; Fukui 2003). The number of seeds per fruit also plays a role in dispersal distance, as gut displacement may in- fluence the rate of seed passage (Stapanian 1982; Levey 1987).
A number of studies have found that fruit and seed morphology may vary ge- ographically (e.g., Cech and Kitzmiller 1968; Hampe and Bairlein 2000; García et al. 2001; Hampe 2003). Despite this fact and the relevance of these traits to fruit choice by birds and subsequent seed dispersal, few compilations of fruit morphology that provide specif ic location-based data exist. As part of a larger study on the use of urban natural areas by birds and of fruits in bird diets (Craves 2009; Craves 2015), I compiled data on the morphological traits of autumn- ripening fleshy fruits of plants in Wayne and Washtenaw counties in southeastern Michigan. I also compiled literature reports of measurements for the same species from other localities.
MATERIALS AND METHODS
I def ine “fruits” here in a functional sense as seed-containing structures with nutritious, fleshy pulp consumed by birds. Depending on the species, fruits may be berries, drupes, pomes, or fleshy cones. Likewise, “seeds” refers to the dispersal unit of the plant, whether it is technically a seed, a stone, an achene, or a similar structure (Stapanian 1982; Willson 1986; Snow and Snow 1988).
This study includes most of the common bird-dispersed, fleshy-fruited plants found in southeast- ern Michigan, comprising native plants as well as non-native plants that occur outside of cultivation (Voss and Reznicek 2012). Plants were considered “bird-dispersed” if birds were observed feeding on their fruits or if their seeds were found in fecal samples collected from banded birds or from seed traps (n>5,900 samples and >38,000 seeds from 22 bird species) as part of a larger study on the role of fruit in bird diets (Craves 2009; Craves 2015).
From 2013 through 2015, fruits were collected for measurements primarily at or near the campus of the University of Michigan-Dearborn, Dearborn, Wayne County, and in section 5 of Lodi Town- ship, Washtenaw County. At least ten ripe fruits of each taxon were collected approximately once a week during the period coinciding with fall bird migration (early to mid-August through early No- vember). In North America, many migratory bird species that are primarily insectivorous feed heav- ily on fruit in fall and winter, and large fruit crops become available to birds at this time (Thompson and Willson 1979; Baird 1980; Willson 1986; Parrish 1997; Jordano 2000). Fruits were collected from the time of f irst ripening until depletion. If fruits remained past early November, they were col- lected until they were depleted, or until the only remaining fruits were dry, shriveled, or malformed; such fruits were not measured. During each sampling session, I chose fruits from multiple plants growing in various conditions, if possible, to reduce the bias that might arise from the variability in fruit or seed size in different years (García et al. 2001; Parciak 2002) or within a single season (Gor- chov 1985; Hernández 2009; but see Eriksson and Ehrlén 1991) or that are caused by differences in maternal environment (Baskin and Baskin 1998; Silander and Klepeis 1999; Schulz and Wright 2015).
Measurements were made on fresh fruits within several hours of collection. Immediately after measuring a fruit, I stripped the pulp from the seeds and counted and measured them. I measured the greatest dimension of each fruit or seed with digital Vernier calipers to the nearest 0.01 mm. Most fruit were globose or nearly so, and thus the greatest dimension was the diameter or width, usually perpendicular to the stalk of the fruit. For elliptical or elongated fruits or seed, the greatest dimension was the length.
Measurements for the same taxa that were collected in southeastern Michigan were compiled from the literature whenever the source indicated that they were obtained in a particular geographic region and provided the mean of the measurements. I searched multiple online databases, websites,
Page 12 12 THE GREAT LAKES BOTANIST Vol. 56
and major scientif ic publishers. I searched for each species by name and also used combinations of plant generic names with terms such as “fruit,” “seed,” “morphology,” or “traits.” Nevertheless, my compilation is not exhaustive.
I measured 5,810 fruits and 8,195 seeds of 37 taxa (Table 1). Fruits and seeds of all these taxa were found in bird fecal samples except for Lindera benzoin, Menispermum canadense, and Solanum ptychanthum (see Table 1 for common names and taxonomy), although birds were occasionally observed eating fruits of these species. Celastrus seeds were found in fecal samples only from Wayne County, where C. scandens is rare, but where C. orbiculatus is abundant. Only f ive species were found in more than ten percent of the fecal samples (and there- fore considered a major dietary component, after Jordano 1988): Lonicera maackii, Rhamnus cathartica, Phytolacca americana, Vitis riparia, and a culti- vated, small-fruited, non-native Malus (crabapple) species. I did not include measurements from fruit or seeds of the latter, since I was unable to determine its parentage, and no individuals of the small-fruited Malus were located outside cultivation.
I located 199 measurements for 33 species in the literature (Table 2). My Ligustrum measurements included fruit from some plants with ambiguous char- acteristics that may have been hybrids, so I included measurements for L. ob- tusifolium and L. vulgare from the literature. I found none of the target measure- ments for Viburnum lentago, Berberis thunbergii, Pyrus calleryana, Rosa setigera, Solanum ptychanthum, or Parthenocissus inserta. For the latter, I sub- stituted measurements found for its close relative P. quinquefolia, since the two species are easily confused and both are often referred to as “Virginia Creeper” (Pringle 2010). Reports of fruit size of six of the species, seed count of three species, and seed size for 21 species were not found.
I describe three important morphological traits—fruit size, seed count, and seed size—for 37 taxa of autumn-ripening, fleshy-fruited, bird-dispersed plants from southeastern Michigan. Measurements for nearly a third of these species are not readily available in the literature. This is surprising considering that a number of them (e.g., Berberis thunbergii, Frangula alnus, Rhamnus cathartica, Pyrus calleryana, Rosa mulitflora, and Ligustrum spp.) are important non-na- tive, invasive species. The success of many fleshy-fruited invasive species is in part due to fruit traits that have facilitated their dispersal by birds (Buckley et al. 2006; Gosper and Vivian-Smith 2010).
The average size of the fruits I measured was just under 8 mm. Average seed count was approximately f ive, and the average greatest dimension of seeds just under 5 mm. These measurements correspond well with those in other compila- tions of bird-dispersed fleshy fruits (Wheelwright 1985; Jordano 1995; Nakan-
Page 13 TABLE 1. Morphometrics ( mean ± SE) of common bird- dispersed, fleshy fruits collected in southeastern Michigan. Fruit and seed sizes are the greatest dimen- sion, usually diameter or width for spherical, and length for non- spherical, fruits and seeds. Species not native to North America are indicated by boldface type. Nomenclature and common names follow Voss and Reznicek ( 2012) , with additional common names from USDA, NRCS ( 2016) . Commonly encountered syn- onyms are indicated in square brackets.
Taxon Fruit size ( mm) Seed count per fruit Seed size ( mm)
CUPRESSACEAE Juniperus virginiana L. , Red Cedar, Eastern Redcedar 5.96± 0.09 ( n= 185) 1.77± 0.06 ( n= 185) 3.49± 0.06 ( n= 190)
ADOXACEAE Viburnum lentago L. , Nannyberry 11.2± 0.07 ( n= 135) 1.00± 0.00 ( n= 135) 9.74± 0.06 ( n= 135) Viburnum opulus L. , European Highbush- Cranberry, Guelder- Rose, European Cranberrybush 10.29± 0.11 ( n= 105) 1.00± 0.00 ( n= 105) 8.27± 0.10 ( n= 105)
ANACARDIACEAE Rhus glabra L. , Smooth Sumac 4.23± 0.06 ( n= 75) 1.00± 0.00 ( n= 75) 3.17± 0.05 ( n= 75) Rhus typhina L. , Staghorn Sumac 5.18± 0.06 ( n= 160) 1.00± 0.00 ( n= 160) 3.61± 0.04 ( n= 140) Rhus combination1 4.88± 0.05 ( n= 235) 1.00± 0.00 ( n= 235) 3.46± 0.03 ( n= 215) Toxicodendron radicans ( L. ) Kuntze, Poison- Ivy, Eastern Poison Ivy 4.37± 0.04 ( n= 110) 1.00± 0.00 ( n= 110) 4.04± 0.04 ( n= 225)
AQUIFOLIACEAE Ilex verticillata ( L. ) A. Gray, Winterberry, Michigan Holly, Black- Alder, Common Winterberry 7.62± 0.06 ( n= 135) 5.13± 0.12 ( n= 135) 4.06± 0.04 ( n= 185)
BERBERIDACEAE Berberis thunbergii DC. , Japanese Barberry 9.92± 0.06 ( n= 150) 1.49± 0.04 ( n= 150) 6.59± 0.04 ( n= 155)
CANNABACEAE Celtis occidentalis L. , Hackberry, Common Hackberry 7.31± 0.03 ( n= 115) 1.00± 0.00 ( n= 115) 6.19± 0.05 ( n= 115)
CAPRIFOLIACEAE Lonicera japonica Thunb. , Japanese Honeysuckle 6.20± 0.08 ( n= 135) 7.70± 0.34 ( n= 135) 3.15± 0.03 ( n= 155) Lonicera maackii ( Rupr. ) Herder, 2 Amur Honeysuckle 6.51± 0.07 ( n= 465) 3.98± 0.10 ( n= 465) 3.90± 0.02 ( n= 820)
2017 THE GREAT LAKES BOTANIST 13
Page 14 TABLE 1. Continued.
Taxon Fruit size ( mm) Seed count per fruit Seed size ( mm)
CELASTRACEAE Celastrus orbiculatus Thunb. , Oriental Bittersweet 6.62± 0.06 ( n= 155) 4.41± 0.11 ( n= 155) 3.98± 0.02 ( n= 205) Celastrus scandens L. , Climbing Bittersweet, American Bittersweet 7.87± 0.10 ( n= 105) 3.19± 0.14 ( n= 105) 5.05± 0.03 ( n= 220) Euonymus alata ( Thunb. ) Siebold, Winged Euonymus, Burningbush 6.36± 0.06 ( n= 130) 1.03± 0.01 ( n= 130) 4.65± 0.03 ( n= 130)
CORNACEAE Cornus amomum Mill. , Silky Dogwood, Pale Dogwood 7.43± 0.06 ( n= 150) 1.00± 0.00 ( n= 150) 5.35± 0.04 ( n= 150) Cornus drummondii C. A. Mey. , Rough- leaved Dogwood, Roughleaf Dogwood 6.04± 0.05 ( n= 150) 1.00± 0.00 ( n= 150) 3.96± 0.04 ( n= 150) Cornus florida L. , Flowering Dogwood 10.63± 0.11 ( n= 75) 1.00± 0.00 ( n= 75) 8.32± 0.09 ( n= 75) Cornus foemina racemosa ( Lam. ) J. S. Wilson. , [ Cornus racemosa Lam. ] Gray Dogwood 6.09± 0.05 ( n= 175) 1.00± 0.00 ( n= 175) 4.75± 0.05 ( n= 175) Cornus sericea L. , [ Cornus stolonifera Michx. ] Red- osier, Redosier Dogwood 7.05± 0.06 ( n= 200) 1.00± 0.00 ( n= 200) 4.83± 0.04 ( n= 200)
ELAEAGNACEAE Elaeagnus umbellata Thunb. , Autumn Olive, Autumn- Olive 7.55± 0.07 ( n= 155) 1.00± 0.00 ( n= 155) 6.79± 0.07 ( n= 155)
LAURACEAE Lindera benzoin ( L. ) Blume, Spicebush, Northern Spicebush 9.12± 0.14 ( n= 50) 1.00± 0.00 ( n= 50) 7.02± 0.11 ( n= 50)
MENISPERMACEAE Menispermum canadense L. , Moonseed, Common Moonseed 9.30± 0.07 ( n= 140) 1.00± 0.00 ( n= 140) 7.94± 0.04 ( n= 140)
OLEACEAE Ligustrum spp. , 3 Privet 6.42± 0.04 ( n= 220) 1.00± 0.01 ( n= 220) 5.89± 0.03 ( n= 220)
PHYTOLACCACEAE Phytolacca americana L. , Pokeweed, American Pokeweed 8.90± 0.05 ( n= 225) 9.29± 0.09 ( n= 185) 3.07± 0.01 ( n= 500)
RHAMNACEAE Frangula alnus Mill. , Glossy Buckthorn 7.61± 0.06 ( n= 200) 2.45± 0.04 ( n= 200) 5.09± 0.05 ( n= 200) Rhamnus cathartica L. , Common Buckthorn 7.34± 0.06 ( n= 255) 3.89± 0.02 ( n= 180) 5.22± 0.03 ( n= 525)
14 THE GREAT LAKES BOTANIST Vol. 56
Page 15 ROSACEAE Crataegus phaenopyrum ( L. f. ) Medik. , Washington Hawthorn, Washington Thorn 7.96± 0.07 ( n= 160) 4.91± 0.05 ( n= 150) 4.55± 0.03 ( n= 195) Pyrus calleryana Decne. , Callery Pear, Bradford Pear 12.49± 0.18 ( n= 115) 2.71± 0.12 ( n= 100) 4.89± 0.06 ( n= 160) Rosa multiflora Murray, Multiflora Rose, Japanese Rose 7.95± 0.10 ( n= 150) 7.57± 0.18 ( n= 150) 3.91± 0.03 ( n= 350) Rosa setigera Michx. , Prairie Rose, Climbing Rose 9.46± 0.10 ( n= 150) 25.84± 0.60 ( n= 120) 4.23± 0.03 ( n= 330)
SMILACACEAE Smilax hispida Raf. , [ Smilax tamnoides L. ] Bristly Greenbriar 7.21± 0.07 ( n= 130) 1.12± 0.03 ( n= 130) 4.92± 0.07 ( n= 125) Smilax lasioneura Hook. , Carrion- flower, Blue Ridge Carrionflower 8.91± 0.10 ( n= 125) 3.62± 0.14 ( n= 125) 4.69± 0.04 ( n= 175)
SOLANACEAE Solanum dulcamara L. , Bittersweet Nightshade, Climbing Nightshade, Woody Nightshade, European Nightshade 9.79± 0.11 ( n= 150) 30.13± 0.70 ( n= 155) 2.46± 0.02 ( n= 360) Solanum ptychanthum Dunal, Eastern Black Nightshade, Black Nightshade 7.04± 0.06 ( n= 115) 56.82± 0.92 ( n= 105) 1.45± 0.01 ( n= 225)
VITACEAE Ampelopsis brevipedunculata ( Maxim. ) Trautv. , Porcelain Vine, Amur Peppervine, Porcelainberry 9.02± 0.09 ( n= 155) 2.53± 0.08 ( n= 155) 4.63± 0.02 ( n= 205) Parthenocissus inserta ( A. Kern. ) Fritsch4 , [ Parthenocissus vitacea ( Knerr) Hitchc. ] Thicket Creeper, Woodbine 7.77± 0.07 ( n= 180) 2.57± 0.08 ( n= 180) 4.49± 0.03 ( n= 275) Vitis riparia Michx. , Riverbank Grape, River- bank Grape 8.45± 0.06 ( n= 225) 2.02± 0.06 ( n= 200) 5.10± 0.02 ( n= 400)
1 Hybridization between the two previous species is common in Michigan ( Voss and Reznicek 2012) , and many samples of R. glabra had some hybrid characteristics. Thus, combined measurements are also provided here. 2 Other common shrub honeysuckles are primarily summer fruiting. 3 Nearly all plants keyed to L. obtusifolium Siebold & Zucc. , Border Privet, but some had characteristics of L. vulgare L. , Common Privet ( Nesom 2009; Maddox et al. 2010; Voss and Reznicek 2012) , so I combined them here. 4 The very similar species P. quinquefolia ( L. ) Planch. is far less common at my study sites and sets fruit much less frequently.
2017 THE GREAT LAKES BOTANIST 15
Page 16 TABLE 2. Available literature reports of morphometrics of fruits of some of the same species in Table 1. Single values are variously described as diameter, size, length, or longest, shortest, or least dimension. If two values are given for fruit or seed size, these are length or longest dimension and width, diameter, or shortest dimension. See source material for details of the measurements. Locations for each source are given as country or US state; the source material usually provides more specific sites. See Table 1 for common names and nomenclature. Species and source Fruit size (mm) Seed count Seed size (mm) Location ADOXACEAE Viburnum opulus Herrera 1987 10.2 x 8.9 (n=20-40) 1.0 (n=20-40) Spain Snow and Snow 1988 9.0 x 8.4 (n=10) 1.0 (n=10) England Eriksson and Ehrlén 1991 9.7 (n=25) 1.0 (n=25) Sweden Englund 1993 9.3 x 8.3 (n=71) Sweden Gervais and Wheelwright 1994 11.0 (n=25) 1.0 (n=25) 7.8 x 7.1 (n=10) Maine, USA Whelan et al. 1998 8.9 (n=10) Illinois, USA Hampe 2003 10.4 Germany Hernández 2009 10.16 x 9.28 (n=390), 7.84 x 6.67 (n=390), Spain early season early season 10.82 x 9.43 (n=390), 8.19 x 6.84 (n=390) late season late season Lee et al. 1991 1.0 (n=200) England CUPRESSACEAE Juniperus virginiana Fassett 1944 4.7 (n=33) Michigan, USA 4.6 (n=142) Massachusetts, USA McPherson 1987 6.15 x 5.35 (n=10) Oklahoma, USA Stapanian 1982 1.67 (n=40) Kansas, USA White 1989 1.2 (n=10) New Jersey, USA ANACARDIACEAE Rhus glabra Stapanian 1982 1.0 (n=40) Kansas, USA White 1989 1.0 (n=10) New Jersey, USA Li 1999 5.44 x 4.84 (n=50) 3.1 x 2.4 (n=80) Kentucky, USA Shelton and Cain 2002 1.0 (n=20) Arkansas, USA 16 THE GREAT LAKES BOTANIST Vol. 56 Page 17 Rhus typhina White 1989 1.0 (n=10) New Jersey, USA Li 1999, Li et al. 1999 2.7 x 2.1 (n=80) Tennessee, USA Toxicodendron radicans Johnson et al. 1985 (as Rhus radicans) 1.0 (n=15) Illinois, USA White 1989 1.0 (n=10) New Jersey, USA AQUIFOLIACEAE Ilex verticillata White 1989 5.8 (n=10) New Jersey, USA Gervais and Wheelwright 1994 7.7 (n=25) Maine, USA CANNABACEAE Celtis occidentalis Stapanian 1982 1.0 (n=40) Kansas, USA Johnson et al. 1985 9.8 (n=30) 1.0 (n=30) Illinois, USA White 1989 1.0 (n=10) New Jersey, USA CAPRIFOLIACEAE Lonicera japonica White 1989 6.7 (n=10) New Jersey, USA Williams and Karl 1996 5.1 (n˜25) 6.1 (n˜100) New Zealand Hidayati et al. 2000 2.89 (n=50) Kentucky, USA Shelton and Cain 2002 6.2 (n=20) Arkansas, USA Kominami et al. 2003 Japan Takahashi and Kamitani 2004 7.7 (n=100) 2.0 Japan Greenberg and Walter 2010 4.3 (n=648) North Carolina, USA Lonicera maackii Whelan et al. 1998 6.7 (n=10) Illinois, USA Hidayati et al. 2000 4.24 (n=50) Kentucky, USA Schulz and Wright 2015 3.1 (n=200), low light Oklahoma, USA 4.4 (n=200), high light (Continued) 2017 THE GREAT LAKES BOTANIST 17 Page 18 TABLE 2. Continued. Species and source Fruit size (mm) Seed count Seed size (mm) Location CELASTRACEAE Celastrus orbiculatus Patterson 1974 2.8 (n=149) North Carolina, US 4.11 (n=163) Virginia, USA 3.89 (n=194) Pennsylvania, USA 2.48 (n=100) New Jersey, USA White 1989 4.8 (n=10) New Jersey, USA Tibbetts 2000 3.68 (n=1,003) Michigan, USA Van Clef 2001 4.9 (n=60) New Jersey, USA Fukui 2003 7.5 (n=20) 3.8 (n=20) Japan Kominami et al. 2003 4.9 2.7 Japan Leicht-Young et al. 2007 4.1 (n=150) Indiana, USA Greenberg and Walter 2010 5.0 (n=642) North Carolina, USA Masaki et al. 2012 7.4 x 7.0 (n=30) 3.7 (n=30) 4.0 x 2.5 (n=30) Japan Celastrus scandens Johnson et al. 1985 4.4 (n=10) Illinois, USA Tibbetts 2000 2.43 (n=390) Michigan, USA Van Clef 2001 3.1 (n=60) New Jersey, USA Leicht-Young et al. 2007 2.8 (n=150) Indiana, USA Euonymus alatus Takahashi and Kamitani 2004, 5.5 (n=100) Japan (as E. alatus f. stiatus) CORNACEAE Cornus amomum Borowicz 1988 4.4 (n=40) Pennsylvania, USA White 1989 1.0 (n=10) New Jersey, USA McCall and Walck 2014 1.0 Tennessee, USA 18 THE GREAT LAKES BOTANIST Vol. 56 Page 19 Cornus drummondii Stapanian 1982 1.0 (n=40) Kansas, USA Whelan et al. 1998 7.4 (n=10) Illinois, USA Cornus florida White 1989 1.0 (n=10) New Jersey, USA Fukui 2003 11.0 (n=20) 5.3 (n=20) Japan Cornus foemina subsp. racemosa Johnson et al. 1985 (as C. racemosa) 6.39 (n=30) 1.0 (n=130) Illinois, USA Borowicz 1988 (as C. racemosa) 4.6 (n=40) Pennsylvania, USA White 1989 (as C. racemosa) 1.0 (n=10) New Jersey, USA Cornus sericea Piper 1986 (as C. stolonifera) 6.16 (n=100) 1.0 (n=50) Washington, USA Traveset et al. 2004 (as C. stolonifera) 1.0 (n=40) Alaska, USA ELAEAGNACEAE Elaeagnus umbellata Nakanishi 1996 5.1 x 5.6 (n=10) Japan Fukui 2003 10.0 (n=20) 6.5 (n=20) Japan Kohri et al. 2010 5.5 x 5.3 (n=20) 1.0 5.4 x 2.8 (n=20) Japan Maskai et al. 2012 8.8 x 8.4 (n=30) 1.0 (n=30) 6.9 x 3.0 (n=30) Japan McCall and Walck 2014 8.8 x 7.57 (n=12) 1.0 (n=12) Tennessee, USA LAURACEAE Lindera benzoin Johnson et al. 1985 8.53 (n=30) 1.0 (n=72) Illinois, USA White 1989 1.0 (n=10) New Jersey, USA MENISPERMACEAE Menispermum canadense Stapanian 1982 1.0 (n=40) Kansas, USA Johnson et al. 1985 7.98 (n=30) 1.0 (n=78) Illinois, USA (Continued) 2017 THE GREAT LAKES BOTANIST 19 Page 20 TABLE 2. Continued. Species and source Fruit size (mm) Seed count Seed size (mm) Location OLEACEAE Ligustrum obtusifolium Nakanishi 1996 6.8 x 5.8 (n=10) Japan Ligustrum vulgare Hererra 1987 7.1 x 6.1 (n=20-40) 1.1 (n=20-40) Spain Snow and Snow 1988 8.5 (n=10) 2.2 (n=10) England Lee et al. 1991 2.5 (n=200) England Obeso and Grubb 1993 1.65 England Shelton and Cain 2002 1.0 (n=20) Arkansas, USA Hampe 2003 7.2 Germany PHYTOLACCACEAE Phytolacca americana Stapanian 1982 9.23 (n=40) Kansas, USA McDonnell et al. 1984 9.85 (n=280) New Jersey, USA Johnson et al. 1985 7.86 (n=30) 9.68 (n=150) Illinois, USA White 1989 9.5 (n=10) New Jersey, USA Whelan et al. 1998 8.9 (n=10) Illinois, USA Prather et al. 2000 8.24 (n=100) Arkansas, USA Fukui 2003 8.0 (n=20) 3.0 (n=20) Japan RHAMNACEAE Frangula alnus Herrera 1987 6.2 x 6.9 (n=20-40) 2.6 (n=20-40) Spain Eriksson and Ehrlén 1991 7.8 (n=25) 2.0 (n=25) Sweden Medan 1994 7.6 x 8.3 (n=17) Spain Hampe and Bairlein 2000 8.3 x 9.0 (n=200) 2.9 (n=200) Spain 7.6 x 8.2 (n=110), early season 2.1 (n=110), early season Germany 7.6 x 8.3 (n=90), late season 2.4 (n=90), late season Germany 20 THE GREAT LAKES BOTANIST Vol. 56 Page 21 Hampe 2003 9.4 Germany Clark 2012 8.31 (n=124) 2.41 (n=124) Massachusetts, USA 9.16 (n=151) 2.65 (n=151) Massachusetts, USA Bolmgren and Eriksson 2015 8.7 (n=458) 1.7 (n=960) Sweden Rhamnus cathartica Herrera 1987 6.3 x 7.4 (n=20-40) 3.5 (n=20-40) Spain Snow and Snow 1988 8.1 x 8.6 (n=10) 4.0 (n=10) England White 1989 3.9 (n=10) New Jersey, USA Lee et al. 1991 3.8 (n=200) England Whelan et al. 1998 8.1 (n=10) Illinois, USA ROSACEAE Crataegus phaenopyrum White 1989 5.0 (n=10) New Jersey, USA Rosa multiflora White 1989 4.6 (n=10) New Jersey, USA Greenberg and Walter 2010 6.5 (n=360) North Carolina, USA SMILACACEAE Smilax hispida Johnson et al. 1985 7.29 (n=30) 1.15 (n=82) Illinois, USA Smilax lasioneura Johnson et al. 1985 7.73 (n=30) 3.31 (n=120) Illinois, USA SOLANACEAE Solanum dulcamara Herrera 1987 11.0 x 7.7 (n=20-40) 27.6 (n=20-40) Spain Snow and Snow 1988 12.2 x 8.6 (n=10) 26.9 (n=10) England Eriksson and Ehrlén 1991 6.2 (n=25) 17.9 (n=25) Sweden (Continued) 2017 THE GREAT LAKES BOTANIST 21 Page 22 TABLE 2. Continued. Species and source Fruit size (mm) Seed count Seed size (mm) Location VITACEAE Ampelopsis brevipedunculata Kominami et al. 2003 5.8 3.4 Japan Parthenocissus quinquefolia Stapanian 1982 2.81 (n=40) Kansas, USA Johnson et al. 1985 7.48 (n=30) 2.1 (n=20) Illinois, USA White 1989 3.0 (n=10) New Jersey, USA Van Clef 2001 3.1 (n=60) New Jersey, USA Vitis riparia Stapanian 1982 2.64 (n=40) Kansas, USA White 1989 2.0 (n=10) New Jersey, USA Whelan et al. 1998 8.3 (n=10) Illinois, USA 22 THE GREAT LAKES BOTANIST Vol. 56 Page 23 2017 THE GREAT LAKES BOTANIST 23
ishi 1996; Flörchinger et al. 2010; Gosper and Vivian-Smith 2010; also summa- rized in Willson 1986). My sample sizes were also often larger than those pro- vided in the literature; 90% of mine were greater than 100, in contrast to fewer than 25% for measurements reported in the literature.
These data can be used in biogeographical studies, which are considered im- portant in understanding demographic processes and how plants adapt to distur- bance or novel environments (Hierro et al. 2005; Wright 2007; Uriarte et al. 2011; Farwig and Berens 2012). In a broader context, knowledge of fruit traits that promote frugivory and subsequent seed dispersal can assist in restoration and conservation efforts by informing managers of how seeds (and thereby the genetic diversity of species) may be dispersed through habitats and alter restora- tion trajectories (Wright 2007; McConkey et al. 2012; McAlpine et al. 2016) and aiding them in assessing risks from undesirable invasive species (Gosper et al. 2005; Buckley et al. 2006; Gosper and Vivian-Smith 2010; Westcott and Fletcher 2011).
A number of authors have stressed the importance of integrating seed disper- sal research, including plant-animal interactions such as the role of frugivorous birds, into conservation practice (Gosper et al. 2005; Wenny et al. 2011; Westcott and Fletcher 2011; McConkey et al. 2012; McAlpine et al. 2016). Based on my literature search, specif ic data on fruit traits is collected in a wide variety of stud- ies. Compilation of these widely dispersed data increases their exposure and of- fers valuable opportunities for new insights and collaborations across disci- plines.
Many thanks to Dana Wloch and Darrin O’Brien for invaluable assistance with collecting fruit, and to W. Kaiser, M. Schwarz, M. Kress, the Gilberts, and Dr. B. J. Murray for funding in support of this research.
Baird, J. W. (1980). The selection and use of fruit by birds in an eastern forest. Wilson Bulletin 92:
63–73. Baskin, C. C., and J. M. Baskin. (1998). Seeds—Ecology, biogeography, and evolution of dormancy
and germination. Academic Press, San Diego, California. Blendinger, P. G., and M. Villegas. (2011). Crop size is more important than neighborhood fruit
availability for fruit removal of Eugenia uniflora (Myrtaceae) by bird seed dispersers. Plant Ecol-
ogy 212: 889–899. Bolmgren, K., and O. Eriksson. (2015). Are mismatches the norm? Timing of flowering, fruiting, dis-
persal and germination and their f itness effects in Frangula alnus (Rhamnaceae). Oikos 124: 639–
648. Borowicz., V. A. (1988). Fruit consumption by birds in relation to fat content of pulp. American Mid- land Naturalist 119: 121–127. Buckley, Y. M., S. Anderson, C. P. Catterall, R. T. Corlett, T. Engel, C. R. Gosper, R. Nathan, et al.
(2006). Management of plant invasions mediated by frugivore interactions. Journal of Applied
Ecology 43: 848–857.
Carlo, T. A. (2005). Interspecif ic neighbors change seed dispersal pattern of an avian-dispersed plant. Ecology 86: 2440–2449. Cech, F. C., and J. H. Kitzmiller, Jr. (1968). Geographic variation in seed and seedling characteristics of black cherry (Prunus serotina Ehrh.). Pp. 53–62 in 15th Northeastern Forest Tree Improvement
Page 24 24 THE GREAT LAKES BOTANIST Vol. 56
Conference Proceedings. Available at https://babel.hathitr ust.org/cgi/pt?id=umn.31951d 004072238;view=1up;seq=65 (Accessed March 15, 2016).
Clark, E. J. (2012). Influence of climate, fruit availability and nutritional content on bird selection of non-native, invasive (Frangula alnus) and native (Prunus serotina) fruit in eastern Massachusetts. M.Sc. thesis, Northeastern University, Boston.
Craves, J. A. (2009). A f ifteen-year study of fall stopover patterns of Catharus thrushes at an inland, urban site. Wilson Journal of Ornithology 121: 112–118.
Craves, J. A. (2015). Birds that eat nonnative buckthorn fruit (Rhamnus cathartica and Frangula alnus, Rhamnaceae) in eastern North America. Natural Areas Journal 35: 279–287.
Denslow, J. S. (1987). Fruit removal rates from aggregated and isolated bushes of the red elderberry, Sambucus pubens. Canadian Journal of Botany 65: 1229–1235.
Englund, R. (1993). Fruit removal in Viburnum opulus: Copious seed predation and sporadic massive seed dispersal in a temperate shrub. Oikos 67: 503–510.
Eriksson, O., and J. Ehrlén. (1991). Phenological variation in fruit characteristics in vertebrate-dis- persed plants. Oecologia 86: 463–470.
Farwig, N. and D. G. Berens. (2012). Imagine a world without seed dispersers: A review of threats, consequences and future directions. Basic and Applied Ecology 13: 109–115.
Fassett, N. C. (1944). Juniperus virginiana, J. horizontalis and J. scopulorum—I. the specif ic char- acters. Bulletin of the Torrey Botanical Club 71: 410–418.
Flörchinger, M., J. Braun, K. Böhning-Gaese, and H. M. Schaefer. (2010). Fruit size, crop mass, and plant height explain differential fruit choice of primates and birds. Oecologia 164: 151–161.
Foster, M. S. (2008). Freeze-frame fruit selection by birds. Wilson Journal of Ornithology 120: 901–
905. Fukui, A. (2003). Relationship between seed retention time in bird’s gut and fruit characteristics. Or- nithological Science 2: 41–48. García, D., R. Zamora, J. M. Gómez, and J. A. Hódar. (2001). Frugivory at Juniperus communis de- pends more on population characteristics than on individual attributes. Journal of Ecology 89: 639–647.
Gervais, J. A., and N. T. Wheelwright. (1994). Winter fruit removal in four plant species in Maine. Maine Naturalist 2: 15–24.
Gorchov, D. L. (1985). Fruit ripening asynchrony is related to variable seed number in Amelanchier and Vaccinium. American Journal of Botany 72: 1939–1943.
Gosper, C. R., and G. Vivian-Smith. (2010). Fruit traits of vertebrate-dispersed alien plants: Smaller seeds and more pulp sugar than indigenous species. Biological Invasions 12: 2153–2163.
Gosper, C. R., C. D. Stansbury, and G. Vivian-Smith. (2005). Seed dispersal of fleshy-fruited inva- sive plants by birds: Contributing factors and management options. Diversity and Distributions 11: 549–558.
Greenberg, C. H., and S. T. Walter. (2010). Fleshy fruit removal and nutritional composition of win- ter-fruiting plants: A comparison of non-native invasive and native species. Natural Areas Journal
30: 312–321. Hampe, A. (2003). Large-scale geographical trends in fruit traits of vertebrate-dispersed temperate plants. Journal of Biogeography 30: 487–496. Hampe, A., and F. Bairlein. (2000). Modif ied dispersal-related traits in disjunct populations of bird- dispersed Frangula alnus (Rhamnaceae): A result of its Quaternary distribution shifts? Ecography
23: 303–613. Hernández, A. (2009). Birds and guelder rose Viburnum opulus: Selective consumption and disper- sal via regurgitation of small-sized fruits and seeds. Plant Ecology 203: 111–122. Herrera, C. M. (1984). A study of avian frugivores, bird-dispersed plants, and their interaction in Mediterranean scrublands. Ecological Monographs 54: 1–23. Herrera, C. M. (1987). Vertebrate-dispersed plants of the Iberian Peninsula: A study of fruit charac- teristics. Ecological Monographs 57: 305–331. Hidayati, S. N., J. M. Baskin, and C. C. Baskin. (2000). Dormancy-breaking and germination re- quirements of seeds of four Lonicera species (Caprifoliaceae) with underdeveloped spatulate em- bryos. Seed Science Research 10: 459–469.
Hierro, J. L., J. L. Maron, and R. M. Callaway. (2005). A biogeographical approach to plant inva- sions: The importance of studying exotics in their introduced and native range. Journal of Ecology
93: 5–15. Page 25 2017 THE GREAT LAKES BOTANIST 25
Hoppes, W. G. (1988). Seedfall pattern of several species of bird-dispersed plants in an Illinois wood- land. Ecology 69: 320–329.
Johnson, R. A., M. F. Willson, J. N. Thompson, and R. I. Bertin. (1985). Nutritional values of wild fruits and consumption by migrant frugivorous birds. Ecology 66: 819–827.
Jordano, P. (1988). Diet, fruit choice and variation in body condition of frugivorous warblers in Mediterranean scrubland. Ardea 76: 193–209.
Jordano, P. (1995). Angiosperm fleshy fruits and seed dispersers: A comparative analysis of adapta- tion and constraints in plant-animal interactions. The American Naturalist 145: 163–191.
Jordano, P. (2000). Fruits and frugivory. Pp. 125–166 in Seeds, the ecology of regeneration in plant communities. 2nd edition. M. Fenner, editor. CABI Publishing. New York, N.Y.
Kohri, M., M. Kamada, and N. Nakagoshi. (2010). Spatial-temporal distribution of ornithochorous seeds from an Elaeagnus umbellata community dominating a riparian habitat. Plant Species Biol- ogy 26: 174–185.
Kominami, Y., T. Sato, K. Takeshita, T. Manabe, A. Endo, and N. Noma. (2003). Classif ication of bird-dispersed plants by fruiting phenology, fruit size, and growth form in a primary lucidophyl- lous forest: An analysis, with implications for the conservation of fruit-bird interactions. Ornitho- logical Science 2: 3–23.
Lee, W. G., P. J. Grubb, and J. B. Wilson. (1991). Patterns of resource allocation in fleshy fruits of nine European tall-shrub species. Oikos 61: 307–315.
Leicht-Young, S. A., N. B. Pavlovic, R. Grundel, and K. J. Frohnapple. (2007). Distinguishing native (Celastrus scandens L.) and invasive (C. orbiculatus Thunb.) bittersweet species using morpho- logical characteristics. Journal of the Torrey Botanical Society 134: 441–450.
Levey, D. J. (1987). Seed size and fruit-handling techniques of avian frugivores. The American Nat- uralist 129: 471–485.
Levey, D. J., T. C. Moermond, and J. S. Denslow. (1984). Fruit choice in neotropical birds: the effect of distance between fruits on preference patterns. Ecology 65: 844–850.
Li, X. (1999). Comparative seed biology of several North American Rhus species (Anacardiaceae). Doctoral dissertation. University of Kentucky, Lexington, Kentucky.
Li, X., J. M. Baskin, and C. C. Baskin. (1999). Seed morphology and physical dormancy of several North American Rhus species (Anacardiaceae). Seed Science Research 9: 247–258.
Maddox, V., J. Byrd, Jr., and B. Serviss. (2010). Identif ication and control of invasive privets (Ligus- trum spp.) in the middle southern United States. Invasive Plant Science and Management 3: 482–
488. Masaki, T., K. Takahashi, A. Sawa, T. Kado, S. Naoe, S. Koike, and M. Shibata. (2012). Fleshy fruit characteristics in a temperate deciduous forest of Japan: How unique are they? Journal of Plant Research 125: 103–114.
McAlpine, C., C. P. Catterall, R. MacNally, D. Lindenmayer, J. L. Reid, K. D. Holl, A. F. Bennett, et al. (2016). Integrating plant-and animal-based perspectives for more effective restoration of bio- diversity. Frontiers in Ecology and the Environment 14: 37–45.
McCall, L. J., and J. L. Walck. (2014). Dispersal characteristics of two native and two nonnative fleshy-fruited sympatric shrubs. Castanea 79: 88–99.
McConkey, K. R., S. Prasad, R. T. Corlett, A. Campos-Arceiz, J. F. Brodie, H. Rogers, and L. Santa- maria. (2012). Seed dispersal in changing landscapes. Biological Conservation 146: 1–13.
McDonnell, M. J., E. W. Stiles, G. P. Cheplick, and J. J. Armesto. (1984). Bird-dispersal of Phyto- lacca americana L. and the influence of fruit removal on subsequent fruit development. American Journal of Botany 71: 895–901.
McPherson, J. M. (1987). A f ield study of winter fruit preferences of Cedar Waxwings. Condor 89: 293–306. Medan, D. (1994). Reproductive biology of Frangula alnus (Rhamnaceae) in southern Spain. Plant Systematics and Evolution 193: 173–186. Moermond, T. C., and J. S. Denslow. (1983). Fruit choice in Neotropical birds: Effects of fruit type and accessibility on selectivity. Journal of Animal Ecology 52: 407–420. Nakanishi, H. (1996). Fruit color and fruit size of bird-disseminated plants in Japan. Vegetatio 123: 207–218. Nesom, G. L. (2009). Taxonomic overview of Ligustrum (Oleaceae) naturalized in North America north of Mexico. Phytologia 91: 467–482.
Page 26 26 THE GREAT LAKES BOTANIST Vol. 56
Obeso, J. R., and P. J. Grubb. (1993). Fruit maturation in the shrub Ligustrum vulgare (Oleaceae): Lack of defoliation effects. Oikos 68: 309–316.
Parciak, W. (2002). Environmental variation in seed number, size, and dispersal of a fleshy-fruited plant. Ecology 83: 780–793.
Parrish, J. D. (1997). Patterns of frugivory and energetic condition in Nearctic landbirds during au- tumn migration. The Condor 99: 681–697.
Patterson, D. T. (1974). The ecology of Oriental bittersweet, Celastrus orbiculatus, a weedy intro- duced ornamental vine. Ph.D. dissertation, Duke University, Durham, N.C.
Piper, J. K. (1986). Seasonality of fruit characters and seed removal by birds. Oikos 46: 303–310.
Prather, J. W., K. G. Smith, M. A. Mlodinow, and C. M. Riley. (2000). Characteristics of some fruit- ing plant species in northwest Arkansas, and the avian assemblages that feed on them. Journal of the Arkansas Academy of Science 54: 103–108.
Pringle, J. S. (2010). Nomenclature of the thicket creeper, Parthenocissus inserta (Vitaceae). The Michigan Botanist 49: 73–78.
Sallabanks, R. (1993). Hierarchical mechanisms of fruit selection by an avian frugivore. Ecology 74: 1326–1336.
Sargent, S. (1990). Neighborhood effects on fruit removal by birds: A f ield experiment with Vibur- num dentatum (Caprifoliaceae). Ecology 71: 1289–1298.
Schulz, K. E., and J. Wright. (2015). Reproduction of invasive Amur honeysuckle (Lonicera maackii) and the arithmetic of an extermination strategy. Restoration Ecology 23: 900–908.
Shelton, M. G., and M. D. Cain. (2002). Potential carry-over of seeds from 11 common shrub and vine competitors of loblolly and shortleaf pines. Canadian Journal of Forest Research 32: 412–
419. Silander, J. A., Jr., and D. M. Klepeis. (1999). The invasion ecology of Japanese barberry (Berberis thunbergii) in the New England landscape. Biological Invasions 1: 189–201. Snow, B,. and D. Snow. (1988). Birds and berries: A Sstudy of an Eecological interaction. Poyser, London, United Kingdom. Stapanian, M. A. (1982). Evolution of fruiting strategies among fleshy-fruited plant species of east- ern Kansas. Ecology 63: 1422–1431. Takahashi, K., and T. Kamitani. (2004). Factors affecting seed rain beneath fleshy-fruited plants. Plant Ecology 174: 247–256. Thompson, J. N., and M. F. Willson. (1979). Evolution of temperate fruit/bird interactions: Pheno- logical strategies. Evolution 33: 973–982. Tibbetts, T. J. (2000). The ecology of the exotic, invasive temperate liana Celastrus orbiculatus (Ori- ental bittersweet). Ph.D. dissertation, Michigan State University, East Lansing. Traveset, A., M. F. Willson, and M. Verdú. (2004). Characteristics of fleshy fruits in southeast Alaska: Phylogenetic comparison with fruits from Illinois. Ecography 27: 41–48. Uriarte, M., M. Anciaes, M. T. B. da Silva, P. Rubim, E. Johnson, and E. M. Bruna. (2011). Disen- tangling the drivers of reduced long-distance seed dispersal by birds in an experimentally frag- mented landscape. Ecology 92: 924–937.
USDA, NRCS. (2016). The PLANTS Database. National Plant Data Team, Greensboro, North Car- olina. Available at http://plants.usda.gov (Accessed March 10, 2016).
Van Clef, M. (2001). Early life stage performance of native and non-native congeners of Polygonum, Celastrus, and Parthenocissus: Assessing methods of screening new plant introductions for inva- sive potential. Ph.D. dissertation, Rutgers University, New Brunswick, N.J.
Voss, E. G., and A. A. Reznicek. (2012). Field manual of Michigan flora. University of Michigan Press. Ann Arbor.
Wenny, D. G., T. L. DeVault, M. D. Johnson, D. Kelly, G. H. Sekercioglu, D. F. Tomback, and C. J. Whelan. (2011). The need to quantify ecosystem services provided by birds. The Auk 128: 1–14.
Westcott, D. A., and C. S. Fletcher. (2011). Biological invasions and the study of vertebrate dispersal
of plants: Opportunities and integration. Acta Oecologica 37: 650–656. Wheelwright, N. T. (1985). Fruit size, gape width, and the diets of fruit-eating birds. Ecology 66: 808–818. Whelan, C. J., K. A. Schmidt, B. B. Steele, W. J. Quinn, and S. Dilger. (1998). Are bird-consumed fruits complementary resources? Oikos 83: 195–205. Whelan, C. J., and M. F. Willson. (1994). Fruit choice in migrating North American birds: f ield and aviary experiments. Oikos 71: 137–151.
Page 27 2017 THE GREAT LAKES BOTANIST 27
White, D. W. (1989). North American bird-dispersed fruits: ecological and adaptive signif icance of nutritional and structural traits. Ph.D. dissertation, Rutgers University, New Brunswick, N.J.
Williams, P. A., and B. J. Karl. (1996). Fleshy fruits of indigenous and adventive plants in the diet of birds in forest remnants, Nelson, New Zealand. New Zealand Journal of Zoology 20: 127–145. Willson, M. F. (1986). Avian frugivory and seed dispersal in eastern North America. Pp. 223–279 in
Current Ornithology, Volume 3, R.J. Johnston, editor. Plenum Press. New York, N.Y. Willson, M. F., A. K. Irvine, and N. G. Walsh. (1989). Vertebrate dispersal syndromes in some Aus- tralian and New Zealand plant communities, with geographic comparisons. Biotropica 21: 133–
147. Willson, M. F., and M. N. Melampy. (1983). The effect of bicolored fruit displays on fruit removal by avian frugivores. Oikos 41: 27–31. Wright, S. J. (2007). Seed dispersal in anthropogenic landscapes. Pp. 599–614 in Seed dispersal, the- ory and its application in a changing world. A. J. Dennis, E. W. Schupp, R. J. Green, and D. A. Westcott, editors. CAB International, Oxfordshire, United Kingdom.