Suitability of native milkweed (Asclepias) species versus cultivars for supporting monarch butterflies and bees in urban gardens

Introduction

Burgeoning interest in ecological landscaping to support pollinators, birds, and other urban wildlife is fueling an enthusiastic and active plant movement (Kendle & Rose, 2000; Tallamy, 2008; Jones, 2019; USFS, 2020; USFWS, 2020) and a robust market for native plant species in the nursery, landscape, and gardening trades (Hanson, 2017; ASLA, 2018; Curry, 2018). Native plants can be defined as those that share an evolutionary history with regional insects and other organisms, whereas non-native or exotic plants evolved someplace other than where they have been introduced (Wilde, Gandhi & Colson, 2015). A compelling ecological argument for prioritizing the locally native flora over otherwise desirable (e.g., non-invasive) exotic species is its greater capacity to support local biodiversity, particularly of co-adapted native insect herbivores that are critical food for higher-order consumers including the many species of terrestrial birds that rear their young partly or wholly on insects (Tallamy & Shropshire, 2009; Burghardt, Tallamy & Shriver, 2009; Narango, Tallamy & Marra, 2018). Native plants also support numerous species of pollen-specialist native bees (Fowler, 2016).

Besides promoting plants of local provenance, the horticultural industry has introduced many native plant cultivars, natural variants of native species that are deliberately collected, selected, cross-bred, or hybridized for desirable traits; e.g., disease resistance, plant stature, leaf color, floral display, or extended bloom period, that can be maintained through propagation (Wilde, Gandhi & Colson, 2015). Although use of cultivars is generally discouraged in ecological restoration projects (Lesica & Allendorf, 1999; Kettenring et al., 2014), they are attractive to consumers seeking novel plants that combine the attributes of natives and ornamentals, and open the door to new introductions and vast market potential (Hanson, 2017; Curry, 2018). Indeed, a survey of nurseries in the Mid-Atlantic region, probably representative of the industry overall, found that only 23% of native plant taxa being marketed are true or “wild type”, the rest being available only as cultivated forms (Coombs & Gilchrist, 2017).

Native plant cultivars are not without controversy, however, even for managed landscapes and gardens. Some environmental organizations decry them, arguing that their mass-marketing and use will diminish the genetic diversity of flora in urban ecosystems that are already degraded by preponderance of exotic ornamental plants, further reducing their capacity to adapt to change, support wildlife, or provide other ecosystem services (Wild Ones, 2013). Cultivar traits that could potentially affect pollinator visitation include conversion of anthers and pistils to petals (“double flowered”), color, size, and shape of flowers, floral density, and possibly plant stature (Comba et al., 1999; Corbet et al., 2001; Ricker, Lubell & Brand, 2019). While some floral traits that humans may find attractive in native cultivars, e.g., double flowers or an unusual color, may decrease the quantity, quality, and accessibility of nectar and pollen, making those plants unattractive or of little value to pollinators (Comba et al., 1999; Garbuzov, Alton & Ratnieks, 2017; Mach & Potter, 2018), other native plant cultivars, and many non-natives, do provide high-quality nectar and pollen and can be equally or more attractive to pollinators as native plant species (Masierowska, 2006; Salisbury et al., 2015; White, 2016; Mach & Potter, 2018; Ricker, Lubell & Brand, 2019). Thus, the value of native cultivars for pollinators must be evaluated on a case-by-case basis (Ricker, Lubell & Brand, 2019).

Compared to studies focused on pollinators, little work has addressed the question of whether native plant cultivars are the ecological equivalent to their parent species in supporting native insect folivores. Breeding for traits that change a plant’s form, foliage color, floral display, or phytochemistry could alter cues used by specialist insects in host recognition or acceptance, perhaps to the extent that the insect no longer recognizes or accepts the cultivar as food (Baisden et al., 2018). Alternatively, because there may be tradeoffs in plants’ allocation of resources to defense or growth, selection for traits such as enhanced floral display may make cultivars more palatable to herbivores by reducing their investment in defenses (Herms & Mattson, 1992). Limited research to date suggests the extent to which that may happen depends on the herbivore in question and the particular characteristics of the cultivar that distinguish it from the parent species (Wilde, Gandhi & Colson, 2015). Some cultivar traits, e.g., leaf variegation or leaves altered from green to red or purple, seem to change host suitability for some insects, whereas selection for other traits seems to make little difference insofar as host use by particular herbivores or biodiversity of folivorous insects supported by those plants (Tencazar & Krischik, 2007; Baisden et al., 2018; Poythress & Affolter, 2018). There is particular need for information on whether cultivars of native plants can be as effective as their parental species for supporting specialist native folivores of conservation concern.

The monarch butterfly (Danaus plexippus L.) is arguably the most well-known and beloved native North American insect (Gustafsson et al., 2015). Every fall, hundreds of millions of monarch butterflies make their long-distance journey south from the United States and Canada to overwintering sites in Mexico and California. Both the eastern and western monarch populations declining (Brower et al., 2012; Malcolm, 2018; Rendón-Salinas, Fajardo-Arroyo & Tavera-Alonso, 2015; Pelton et al., 2019) fueling concern that it may face extirpation unless habitat conservation are enacted across North America. Planting milkweeds (Asclepias spp.), the monarch’s obligate larval host plants, is a key part of the international conservation strategy to return this iconic butterfly to sustainable status (Thogmartin et al., 2017; Monarch Joint Venture, 2020; USFWS, 2020). Restoring sufficient milkweed to ensure a stable monarch population will likely require contributions from all land use sectors including urban and suburban areas (Thogmartin et al., 2017; Johnston et al., 2019). In cities and towns, many initiatives are underway, with myriad gardens being planted in residential, educational, and recreational properties (Phillips, 2019; MonarchWatch, 2020; National Pollinator Garden Network, 2020). Milkweed flowers produce abundant nectar and, in addition to monarchs, are highly attractive to bees and numerous other native insects including butterflies, moths, skippers, beetles, and flies (Robertson, 1891; Macior, 1965; Borders & Lee-Mäder, 2015; Baker & Potter, 2018) so urban butterfly gardens can also play a role in supporting their biodiversity. Conservation gardens also provide urban citizens with the opportunity to reconnect with the natural world, helping to foster a greater awareness of conservation issues (Goddard, Dougill & Benton, 2010; Lepczyk et al., 2017; Bellamy et al., 2017).

Native plant cultivars, including milkweeds selected for novel floral display, longer blooming duration, compact growth form, and other consumer-attractive traits, are increasingly available in the wholesale nursery trade and at local garden centers (Baumle, 2018) so it is important to determine if such plants have equivalent value as native species if used for ecological gardening. Different species of milkweeds present a spectrum of palatability across the monarch’s host range (Erickson, 1973; Schroeder, 1976; Baker & Potter, 2018). Milkweed cultivars within a single parental species group may offer a similar spectrum. In this study, we used the high-profile system of milkweeds, monarch butterflies, and bees to test the hypothesis that commercial cultivars provide equivalent ecological benefits as wild-type milkweeds in the context of small urban gardens.

Materials & Methods

Garden study site

Six replicated gardens (1.22 × 9.75 m) were established in public areas of the Arboretum State Botanical Garden of Kentucky, Lexington, in May 2018. The surrounding landscape consisted of restored prairie, formal gardens, and trees. Patches of open, low-maintenance grassland were sprayed with glyphosate to kill existing vegetation, tilled, and covered with weed barrier cloth. Each garden was subdivided into eight randomized 1.22 × 1.22 m plots, one for each of eight milkweed types which included Asclepias incarnata L. (swamp milkweed) and Asclepias tuberosa L. (butterfly milkweed) grown from seedlings produced from commercial open-pollinated seed production fields and hereafter called “wild type” for convenience, and three additional cultivars of each species including A. incarnata ‘Cinderella’, ‘Ice Ballet’, and ‘Soulmate’, and A. tuberosa ‘Blonde Bombshell’, ‘Gay butterflies’ and ‘Hello Yellow’, produced via controlled pollination or tissue culture (Fig. 1, Table S1). The milkweeds were purchased from various producers (American Meadows, Shelburne, VT; Centerton Nurseries, Bridgeton, NJ; Prairie Moon, Winona, MN) as bare root 2-year old plants which were started in our greenhouse. Four plants of a single type (16–30 cm height, depending on species and cultivar) were transplanted 0.6 m apart within each plot. Each garden was then covered with dark brown hardwood mulch (five cm depth). Plants were watered twice per week for the first three weeks to aid establishment and during a period of drought in 2019. We replaced a few of the less-vigorous milkweeds with healthier greenhouse-grown transplants in May 2019 at the start of the second growing season.

Results

Bee assemblages of garden milkweeds

Five families and 17 genera were represented amongst the total of 2436 bees sampled from milkweed blooms in the replicated garden plots (Table 3). Within the A. incarnata group, bee genus diversity was similar (F_3,15 = 1.74, P = 0.2) but genus richness was greater for ‘Soulmate’ than for the wild type (F_3,15 = 4.14, P = 0.03; Table 3). Bee genus diversity was similar within the A. incarnata group ( F_3,15 = 1.74, P = 0.2, Table 3). Bee assemblages of A. incarnata were dominated by Apid bees (Fig. 2), particularly bumble bees (Bombus spp.), carpenter bees (Xylocopa spp.), and honey bees (Apis mellifera). Representation of particular families and genera was similar among the four types except for ‘Soulmate’ which attracted proportionately few Bombus spp. compared to the wild type (χ² = 29.5, P <  0.001).

Table 3:

Bee assemblages of two species of native milkweeds and their cultivars in replicated gardens based on total collected across all sampling dates.

	A. incarnata and cultivarsa				A. tuberosa and cultivarsb
	WT	CN	IB	SM		WT	BB	GB	HY
Andrenidae
Andrena sp.	0	1	0	0		0	0	0	0
Apidae
Apis mellifera	16	60	47	52		27	31	79	29
Bombus bimaculatus	0	12	0	2		6	1	5	9
B. griseocollis	137	213	165	110		41	9	117	75
B. impatiens	0	1	5	0		4	3	29	16
B. pensylvanicus	0	0	0	1		0	0	0	0
Ceratina sp.	0	0	0	0		2	0	11	4
Xylocopa virginica	82	80	32	104		5	0	5	3
Colletidae
Hylaeus sp.	2	3	2	14		0	6	1	0
Halictidae
Agapostemon sp.	0	2	1	1		2	1	8	1
Augochlora sp.	1	0	0	1		10	11	16	4
Augochlorella sp.	0	4	0	6		1	5	15	1
Augochloropsis sp.	1	6	9	15		8	3	7	5
Halictus sp.	0	2	3	0		5	15	5	0
Lasioglossum sp.	11	20	24	39		83	224	91	45
Sphecodes sp.	0	0	1	0		0	0	0	0
Megachilidae
Anthidium sp.	0	0	0	0		4	0	2	2
Coelioxys sp.	0	0	0	1		10	1	10	3
Heriades sp.	0	0	0	0		4	0	0	1
Megachile sp.	0	0	3	3		14	6	35	6
Total bees sampled	250	404	291	346		227	317	398	203
Mean genus richness(SE)	4.5 (0.2)	5.3 (0.6)	6.2 (0.7)	7.0*(0.5)		7.7 (1.0)	6.3 (1.0)	10.0 (0.6)	6.5 (0.4)
Mean genus diversityc (SE)	0.59 (0.04)	0.61 (0.08)	0.63 (0.03)	0.74 (0.04)		0.74 (0.11)	0.46 (0.07)	0.75 (0.02)	0.83 (0.02)

DOI: 10.7717/peerj.9823/table-3

Notes:

aWT, Wild Type; CN, ‘Cinderella’; IB, ‘Ice Ballet’; SM, ‘Soulmate’.

bWT, Wild Type; BB, ‘Blonde Bombshell’, GB, ‘Gay Butterflies’, HY, ‘Hello Yellow’

cSimpson Index of Diversity 1-D (Magurran, 20014) calculated across all six gardens.

*Cultivar mean differs significantly from mean for wild type (Dunnett’s test, P < 0.05). See text for ANOVA results for genus richness and diversity.

Asclepias tuberosa attracted a somewhat more even distribution of bee families and genera, with proportionately more Halictidae and Megachilidae compared to the A. incarnata group, and each cultivar attracting diverse bee genera in varying proportions (Table 3, Fig. 3). Although A. tuberosa ‘Blonde Bombshell’ attracted bees from 11 different genera, most (71%) of them were Halictidae, genus Lasioglossum, accounting for that cultivar having lower genus diversity than the wild type (F_3,15 = 5.82, P = 0.007). There was significant variation in bee genus richness within the A. tuberosa group (F_3,15 = 6.31, P <  0.01) but none of the cultivars had higher or lower richness than did the wild type (Table 3).

Discussion

A major challenge to scaling up the use of native species in landscaping and gardening is providing plants that are both ecologically functional and profitable for the horticulture industry (Wilde, Gandhi & Colson, 2015). Native plants are mainly introduced into urban ecosystems through a market system that satisfies consumer preferences for ornamental traits. Consequently, many native plant species have been selected or bred for extended flowering, novel color, size, or morphology of flowers or foliage, compactness, or other aesthetic characteristics, with frequent new cultivar introductions (Wilde, Gandhi & Colson, 2015). Depending on their traits, some native plant cultivars seem to support specific folivorous insects, or insect-based food webs, as effectively as native plant species, whereas others do not (e.g., Tencazar & Krischik, 2007; Baisden et al., 2018; Poythress & Affolter, 2018; Ricker, Lubell & Brand, 2019). There is particular need for information on whether or not cultivars can support native insects of conservation concern.

Among such insects, none approaches the power of the monarch butterfly as a catalyst for public interest in ecological gardening (Gustafsson et al., 2015). Our results suggest that, at least in urban pollinator gardens, cultivars of A. incarnata and A. tuberosa, two of the most widely-sold garden-friendly native milkweeds (Baker & Potter, 2018), are as suitable as their respective parental species for attracting and supporting monarch butterflies. Over two growing seasons, we found similar numbers of naturally-occurring eggs and larvae on cultivars and straight species within each group. Despite some differences in plant defensive characteristics (trichomes, latex, and cardenolides), larval growth, development, and survival were similar on milkweeds within each group. Monarch larvae are capable of dealing with a range of milkweed defenses (Dussourd & Eisner, 1987; Agrawal & Fishbein, 2006). It is not unexpected, therefore, that cultivation at least within A.incarnata and A. tuberosa does not result in changes in defense that are too severe for monarch larvae to overcome.

Shared evolutionary history with plants has led to widespread host specificity in phytophagous insects (Bernays & Graham, 1988). Many Lepidoptera have narrow host ranges, often restricted to a single genus (Dyer et al., 2007), so a plant breeder selecting for modified plant phenotypes could potentially alter the cues such insect specialists rely upon to recognize their hosts. Butterflies, in general, use a combination of visual, olfactory, and gustatory cues to find and accept host plants (Renwick & Chew, 1994). Monarchs move extensively between habitat patches, but the relative distance over which they use vision or olfaction to locate milkweeds or nectar sources is uncertain (Zalucki, Parry & Zalucki, 2016).

Monarch females foraging in natural habitat tend to lay more eggs on taller, more isolated milkweed plants than on shorter, less accessible ones (Zalucki & Kitching, 1982; Zalucki, Parry & Zalucki, 2016), and the same patterns occur in butterfly gardens (Baker & Potter, 2018; Baker & Potter, 2019). The relatively short stature of all cultivars of A. tuberosa (Table S2) compared to A. incarnata may account, in part, for why we found fewer eggs and larvae on the former species in both years despite them both being suitable as larval food (Erickson, 1973). Shorter milkweeds may go unnoticed by the butterflies because they are less visually apparent and accessible than taller milkweeds, especially when surrounded by non-host plants (Baker & Potter, 2019).

Some other butterfly species form a visual search image for host plants with a particular leaf shape that facilitates host-finding in the field (Benson, Brown & Gilbert, 1975; Rausher, 1978; Dell’Aglio, Lasada & Jiggins, 2016), but it is not known if monarchs do this. The estimated 100 milkweed species native to North America vary in leaf size and shape (Woodson Jr, 1954), and several studies suggest that those with narrow leaves (e.g., A. verticillata) are less preferred for oviposition (Baker & Potter, 2018; Pocius et al., 2018). All native cultivars used in our study had leaves seemingly similar to their parental species, but if plant breeders were to select for cultivars having modified leaf shape, color, or variegation, such changes could potentially affect monarchs’ visual perception of them as hosts.

Native bee populations are declining (Cameron et al., 2011; Koh et al., 2016) and millions of urban pollinator gardens are being planted to help their plight (Phillips, 2019). Milkweed flowers produce abundant nectar (Wyatt & Broyles, 1994), and are highly attractive to bees and other nectar-feeding insects (Fishbein & Venable, 1996; MacIvor et al., 2017; Baker & Potter, 2018). Because milkweed pollen is enclosed within pollinia, nectar is the only reward that milkweeds offer their pollinators (Wyatt & Broyles, 1994). Large bees and wasps are the most effective milkweed pollinators, whereas most of the smaller visitors are unable to transfer pollina and do not provide pollination services to milkweed (Kephart, 1983; Ivey, Martinez & Wyatt, 2003; MacIvor et al., 2017).

In the present study, large-bodied, eusocial Apidae dominated the bee assemblages of A. incarnata whereas A. tuberosa attracted proportionately more Halictidae, Megachilidae, and other relatively small native bees. Both patterns are consistent with an earlier study in which only wild-type milkweeds were compared (Baker & Potter, 2018). Large apid bees have high energy demands (Heinrich, 1976), so may favor milkweeds such as A. incarnata having large flowers and abundant nectar rewards, whereas the relatively smaller flowers of A. tuberosa may provide a sufficient nectar reward for relatively smaller native bees (Baker & Potter, 2018). Unlike garden plants wherein cultivar selection has reduced or eliminated floral rewards for pollinators (Garbuzov, Alton & Ratnieks, 2017; Erickson et al., 2019), all of the native milkweed cultivars we evaluated were bee-attractive. Moreover, with the possible exception of A. tuberosa ‘Blonde Bombshell’ which attracted an inordinately high number of Lasioglossum sp., bee assemblages of the milkweed cultivars were generally similar to those of their respective parental species.

Conclusions

Restoration ecologists, conservation groups, and U.S. federal and state agencies are promoting increased use of native plants in landscaping and gardening to help support biodiversity in urbanized areas. A major challenge to that goal is availability of native plants that satisfy requirements for ecological function, cost-effective production, and desirable ornamental characteristics with consumer appeal. Breeding, marketing, and use of native plant cultivars is widespread and growing in the horticulture industry. This study suggests that, at least in small gardens, native milkweed cultivars can be as suitable as their parental species for attracting and supporting monarch butterflies and native bees. Although probably not appropriate for use in natural areas where maintaining a reservoir of genetic variability is important for plant population resilience, use of native milkweed cultivars in pollinator gardens can help support the urban public’s contribution to monarch and native bee conservation. For urban gardens, planting several species of native milkweeds, regardless of whether they are wild types or native cultivars, plus a variety other plants to provide nectar and pollen throughout the growing season, is probably the best strategy for helping to support monarchs, bees, and other pollinators.

Supplemental Information