Japanese Chaff Flower) Is a Relatively New, Invasive Species to the United States, with Limited Information on Its Life History Characteristics

Research Article

Do plant traits predict the competitive abilities of closely related species?

Lauren M. Schwartz1,3*, David J. Gibson1 and Bryan G. Young2 1 Department of Plant Biology, Center for Ecology, Southern Illinois University, Carbondale, IL 62901, USA

2 Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907, USA Downloaded from 3 Present address: Department of Crop, Soil, and Environmental Sciences, University of Arkansas, Fayetteville, AR 72704, USA Received: 21 August 2015; Accepted: 10 December 2015; Published: 31 December 2015 Associate Editor: James F. Cahill Citation: Schwartz LM, Gibson DJ, Young BG. 2016. Do plant traits predict the competitive abilities of closely related species? AoB PLANTS 8: plv147; doi:10.1093/aobpla/plv147 http://aobpla.oxfordjournals.org/

Abstract. Invasive species are a threat to every ecosystem. There is a strong incentive to predict which species will become invasive before they become too widespread and unmanageable. Different approaches have been advocated to assess invasive species potential. These include examining plant functional traits, quantifying competitive ability and phylogenetic comparison. In this study, we conducted experiments based on the above approaches in a multi-year, temporally replicated, set of experiments to compare these assessment methods to determine the invasive potential of Japanese chaff ﬂower (Achyranthes japonica). We compared plant traits and competitive ability of Japanese chaff

flower with two agricultural invasive species, Palmer amaranth (Amaranthus palmeri) and tall waterhemp (Amaranthus at Arkansas Multisite on January 21, 2016 tuberculatus), and one endangered plant species, bloodleaf (Iresine rhizomatosa), in the Amaranthaceae. Additionally, we assessed the invasive potential based on each of these approaches and determined the degree of agreement between them. A relatively conservative assessment integrating all three approaches would be that the competitive ability of closely related individuals with similar functional traits would share invasive potential. In a greenhouse experiment, each of the study species and soya beans were grown as monocultures and were evaluated to assess the drawdown of an aboveground (light) and a belowground (nitrogen) resource. In a field experiment, each study species was grown at varying densities per 15-cm-diameter pot with or without one or two soya bean plants, to simulate relative densities for soya beans grown in 38- and 76-cm-wide row spacing, respectively. In addition, Japanese chaff flower seedlings were planted either as un-manipulated seedlings or as a seedling cut back to the soil surface at the four-node stage (cut Japanese chaff flower) at which point seedlings have reached a perennial growth stage. The greenhouse experiment showed that each species drew down light differently, but not nitrogen. Shading decreased the aboveground biomass of the species in comparison with unshaded controls. Nitrogen, however, increased the aboveground biomass of Palmer amaranth and Japanese chaff flower. In the field experiment, a competitive effect ranking was determined to be: tall waterhemp Palmer amaranth cut Japanese chaff flower uncut Japanese chaff flower bloodleaf, with the com- ≥ ¼ ≥ ≥ petitive response ranking being the inverse. These results suggest that under specific conditions, these closely related species do exhibit similar competitive abilities. Furthermore, the invasiveness and not the life history or habitat of these closely related species appeared to be the driving factor of competitiveness.

Keywords: Amaranthaceae; competition; early vegetative growth; invasive species; resource drawdown.

* Corresponding author’s e-mail address: [email protected]

Published by Oxford University Press on behalf of the Annals of Botany Company. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properlycited.

AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015 1 Fact Sheet: Ecology and Control of Japanese Chaf Flower

[Achyranthes japonica (Miq.) Nakai] Background Japanese chaf fower (Amaranthaceae) is a relatvely new exotc species that is natve to the eastern and south- eastern regions of Asia. This perennial herbaceous plant was frst found in North America in 1981 along the Tug Fork River in Martn County, Kentucky and has since spread down the Ohio River and its tributaries. Today, this species has been confrmed in 9 states and over 50 countes. The actual distributon of chaf fower in the United States is most likely underestmated due to the lack of public awareness. Water and animals, which includes birds, deer, and people, are the primary cause of spread. The longevity of Japanese chaf fower seed in the soil is unknown, but it is believed that the seeds can remain viable for a number of years. Impacts/Characteristcs High germinaton rate (~62% in drought years and ~94% in average years) High seed output (up to ~2,000/plant) ~ 60% of seedlings survive to produce seed in frst year Produces over 80 stems/m2 (~16,000 seeds) Similar compettve capabilites of other species in the same family (i.e., Palmer amaranth (Amaranthus palmeri) or common waterhemp (Amaranthus tuberculatus)) Contnual fushes of germinaton Outcompetes natve and invasive species (i.e., Japanese stltgrass (Microstegium viminuem)) Current distributon of Japanese chaf fower Allows very litle to no undergrowth due to dense canopy (map courtesy of www.eddmaps.org). Grows in areas with partal sun and moist soils, but can also grow in heavily shaded and dry areas Found in botomland and upland forests, along riverbanks, along agricultural feld margins, and in roadside ditches

Phenology Japanese chaf fower starts growing in late spring and fowers in the late summer. Flowers can contnue to develop into the early fall, even when seed is startng to be produced. The seeds are Progression of seed development mature in mid- to late-fall. As the plants die of in late fall or early (Photo by Travis Neal). winter the stems and remaining seed turn an orange-brown color. The dead plant stand can remain erect even into the winter untl heavy snow, ice, or foods cause the stems to break.

Descripton Perennial, herbaceous species (becomes perennial at three or four nodes) Grows up to three meters tall Leaves: opposite and simple Lopseed surrounded by Japanese chaf fower (Photo by Karla Gage). Stem: red at ground level (as well as the nodes) Flowers: erect spikes at the end of the stems and upper Commonly Misidentfed Species: branches (botle-brush appearance) lopseed (Phryma leptostachya) Fruits: two stf bracts aid in dispersal by ataching to hophornbeam copperleaf clothing, shoes, hair, or animal feathers/fur (Acalypha ostryifolia)

Mechanical Control: Infestatons with chaf fower having four nodes or less can be controlled by hand pulling the above ground plant and roots. It is not recommended to atempt to control perennial populatons by hand pulling alone due to chaf fower’s ability to resprout with increased branching and seed producton. In situatons where populatons of chaf fower are located along hiking trails, road sides and in urban areas, weed eatng and mowing could be a good opton to remove fowering heads and temporarily delay seed release. However, follow- up treatments with systemic herbicides are required to eliminate the plants. Chemical Control: All of the chemicals tested below are systemic herbicides designed to kill the aboveground plant as well as the perennial growth. The herbicides tested were all efectve in the control of chaf fower when sprayed as a 2% soluton in water. A non-ionic surfactant can be added to the soluton to help herbicide absorp- ton by the plant. Always read and follow the herbicide label. If making applicatons near standing water, aquatc- safe herbicides and surfactants must be used and an EPA NPDES permit may need to be obtained. Take every precauton to prevent impact to non-target plants in sensitve forestry sites. Aminopyralid may damage legumi- nous trees and certain evergreens. Applicators may exceed the 7/14 f. oz./acre rate limit if not careful. Of- target drif should always be a concern regardless of the chemical. Always read and follow the herbicide label; the label is the law. Chemical Name Trade Name Aquatc Safeness Herbicide Selectvity Manufacturer 2,4-D ester Various Do not apply to Selectve: Broadleaf Various standing water triclopyr amine Various Labeled for Selectve: Broadleaf Various aquatc use glyphosate Various Some labeled for Nonselectve Various aquatc use aminopyralid Milestone Do not apply to Selectve: Broadleaf Dow AgroSciences LLC Indianapolis, IN Specialty® standing water www.dowagro.com triclopyr and fu- PastureGard Do not apply to Selectve: Broadleaf Dow AgroSciences LLC Indianapolis, IN roxypyr HL® standing water www.dowagro.com aminopyralid and Opensight Do not apply to Selectve: Broadleaf Dow AgroSciences LLC Indianapolis, IN metsulfuron Specialty® standing water www.dowagro.com Actvites such as hiking and huntng can spread chaf fower seed. Make sure to thoroughly clean all seeds of of your clothing, equipment and pets if you are hiking, camping, or huntng in an area where this species occurs.

Reportng If you fnd any populatons of Japanese chaf fower, please contact the River to River CWMA (618-998-5920; [email protected]) or your local extension ofce, and alert other land managers in your area. Use resources like EddmapS (www.eddmaps.org) to check the current distributon of this species and to report any populatons that you come across. ______Citaton: Schwartz LM, KM Smith, C Evans, KL Gage, DJ Gibson, and BG Young. 2015. Fact Sheet: Close up of leaf orientaton and seed Ecology and Control of Japanese Chaf Flower [Achyranthes japonica (Miq.) Nakai]. htp:// head (Photo by Chris Evans). www.rtrcwma.org/Chaf_FactSheet.pdf

The authors would like to acknowledge Southern Illinois University, Carbondale and the Department of Plant Biology for their support; as well as, Dow AgroSciences and Cypress Creek Natonal Wildlife Refuge for chemicals.

Japanese chaf fower seedling. Infestaton of Japanese chaf fower. Achyranthes japonica: A new invader

Lauren M. Schwartz David J. Gibson Outline

• Achyranthes japonica

• Distribution

• Research at SIUC

• What we know

• Ongoing Research

• Things to Remember! Achyranthes japonica (Miq.) Nakai • Amaranthaceae • Perennial • Herbaceous • Reaches 3 meters tall • Native range: Korea, Japan and China • Habitat: Marshes, wetlands and rice paddies • Used and studied in Asian food and drug industry • Continual germination

(Evans 2010, Evans & Taylor 2011, Schwartz 2014) Achyranthes japonica

• Previous ecological studies Invasive on Korean Island (Pearson 2010, Choi et al. 2010) Entangling native Swinhoe’s storm-petrels • Mode of Transport Epizoochory 2 stiff bracts on seed Attaches to fur, feather, clothing Hydrochory Population following river floodplains • Allelopathy Korean rice paddy weed High levels of phenol (Kim 1993)

Dan Pearson Achyranthes japonica

Travis Neal RTRCWMA Current Distribution 1995 Louisville, KY 2008 Massac County, IL 1981 Martin County, KY 2011 Mississippi County, MO

Gibson Lab

• Currently the only lab studying A. japonica Gibson Lab Research on A. japonica • Seed viability/germination rate • Vector transport • Susceptibility to herbicides • Effects of herbivory • Population dynamics • Use of resources • Competitive effects/responses Research: Lindsay Shupert

Achyranthes japonica

350 100 Chestnut Hills 2012 2013 90 Cypress Creek 300

80 250 70

200 60 Chestnut Hills Cypress Creek

150 50 Log % survivorship % Log 100 40

Average Number of Seeds/Plant Number Average 50 Flowering Flowered Died Died 30 0 0 50 100 150 200 250 Chestnut Hills Cypress Creek Days Site • 57% seedling survivorship • 98% germination; high fecundity Research: Travis Neal

• Dispersal vectors – White tailed deer – Turkey feather – Clothing

A. japonica seed

Research: Katie Smith

• Herbicide titration on plants with 3 nodes • 6 herbicides • Field and greenhouse experiments Herbicide Active Mode of Action Field Rate Used Ingredient (2% equivalent) Radar LV® 2,4-D Ester Synthetic Auxin 1,264.91 g ai/ha

Element 3A Triclopyr Synthetic Auxin 1009.123 g ai/ha Specialty®

Bullzeye® Glyphosate Amino Acid 1,345.40 g ai/ha Synthesis Inhibitor

Milestone Aminopyralid Synthetic Auxin 672.8 g ai/ha Specialty®

PastureGard Triclopyr + Synthetic Auxin+ 1,345.68 g ae/ha HL® Fluroxypyr Synthetic Auxin

Opensight Aminopyralid + Synthetic Auxin+ 240.36 g ae/ha Specialty® Metsulfuron Amino Acid Synthesis Inhibitor Results 0.03 a 0.025 /ha)

ai 0.02

0.015

0.01 50 value (g 50 value - b

GR b 0.005 b b b

Herbicide

Bullzeye requires significantly more chemical to reduce growth by 50% Element 3A requires the least amount of chemical Research: Lauren Schwartz

600

) 500 -1 m -1

400 mols

300 BL CF 200 WH PA SB

Light at Light Soil Surface ( 100

0 0 5 10 15 20 Total Nitrogen (mg) C=Control WH=Waterhemp (A. rudis) BL=Bloodleaf (I. rhizomatosa) PA=Palmer amaranth (A. palmeri) CF=Chaff flower (A. japonica) SB=Soybean (G. max) Research: Lauren Schwartz

600

) 500 -1 m -1

400 mols

300 BL CF 200 WH PA SB

Light at Light Soil Surface ( 100

60% Shade 0 No Shade 0 5 10 15 20 Total Nitrogen (mg) C=Control WH=Waterhemp (A. rudis) BL=Bloodleaf (I. rhizomatosa) PA=Palmer amaranth (A. palmeri) CF=Chaff flower (A. japonica) SB=Soybean (G. max) Aboveground Biomass

Nitrogen Treatment Shading Treatment

2.5 3.0 Without N Addition Without Shade N Addition Under 60% Shade * 2.5 2.0 F = 2.19, P = 0.0799 4,64 F4,64 = 3.94, P = 0.0064

2.0 1.5

1.5

1.0 1.0 * * * * * Aboveground Biomass (g) Biomass Aboveground 0.5 0.5

0.0 0.0 WH PA CF BL SB WH PA CF BL SB Species Species

C=Control WH=Waterhemp (A. rudis) BL=Bloodleaf (I. rhizomatosa) PA=Palmer amaranth (A. palmeri) CF=Chaff flower (A. japonica) SB=Soybean (G. max) Belowground Biomass

1.4

Without N Addition/Without Shade a Without N Addition/Under 60% Shade 1.2 N Addition/Without Shade N Addition/Under 60% Shade 1.0 F4,64 = 3.68, P = 0.0092 b

0.8

0.6 c

c 0.4

Belowground Biomass (g) Biomass Belowground a

0.2 a b ab a NS a c bc b b b ab 0.0 WH PA CF BL SB Species C=Control WH=Waterhemp (A. rudis) BL=Bloodleaf (I. rhizomatosa) PA=Palmer amaranth (A. palmeri) CF=Chaff flower (A. japonica) SB=Soybean (G. max) Amaranthus palmeri 5 F = 7.15 1,11.5 Response to Soybeans: Height P = 0.0209 A 4 (cm)

B 3

Height (cm) 2 Amaranthus rudis

12 1 F6,88.7 = 8.92 P < 0.0001 10

0 Achyranthes japonica

Soybeans Present Soybeans8 Absent 2.5 F3,15.1 = 4.06 A P = 0.0267 6 2.0

Height (cm) B 4 1.5 B

2 C BC C C

Height (cm) 1.0 C 0 15 18 21 24 27 30 33 Days After Planting 0.5

Soybeans Present Soybeans Absent 0.0 Soybeans Present Soybeans Absent

Density 1 Density 2 Density 4 Density 8 Mycorrhizal? Ashley Bergman

Putative hyphae. X1000 Trypan blue stain.

Putative vesicles. X400 Trypan blue stain. What We Know • ~95% germination rate/60% survival rate – Depends on previous year’s weather • High fecundity (132 ± 20 seeds per plant) • 2% herbicide solution achieves complete plant death in field • Regrows at the 3 node stage – Becomes perennial VERY early • Increased N and light = increased biomass • Uses resources comparably to agriculture weeds – But not a strong competitor with crop present • Mycorrhizal? Allelopathic? Ongoing Research

• Population dynamics

• Morphological variation across invaded range

• Lightwave filtration (Christa Shen, REU)

• Competitive effects/responses If all else fails…Remember this! • A. japonica seed attaches to everything! – Seed produced in the fall (hunting/hiking)

• High fecundity/viability – EDRR

• Herbicide IS an effective control method – Very low use rate (2% of 1x field rate) Acknowledgements • Katie Smith • Lindsay Shupert • Travis Neal • Karla Gage • Chris Evans • Dr. Bryan Young • IDNR • Dow AgroSciences • Cypress Creek NWR • Department of Plant Biology • Department of Plant, Soil, and Agricultural Systems

Using integral projection models to compare population dynamics of four closely related species

Lauren M. Schwartz, David J. Gibson & Bryan G. Young

Population Ecology

ISSN 1438-3896

Popul Ecol DOI 10.1007/s10144-016-0537-2

1 23 Your article is protected by copyright and all rights are held exclusively by The Society of Population Ecology and Springer Japan. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”.

1 23 Author's personal copy

Popul Ecol DOI 10.1007/s10144-016-0537-2

ORIGINAL ARTICLE

Using integral projection models to compare population dynamics of four closely related species

1 1 2 Lauren M. Schwartz • David J. Gibson • Bryan G. Young

Received: 10 April 2015 / Accepted: 12 January 2016 Ó The Society of Population Ecology and Springer Japan 2016

Abstract Demographic processes, such as survival, the perennial species; whereas, for the annual species growth, and reproduction, can inform us about invasion population dynamics were driven primarily by fecundity. risk, extinction risk, and trade-offs in life history strate- Overall, Achyranthes japonica and the Amaranthus spe- gies. The population dynamics of four Amaranthaceae cies show similar trends in demographic processes that species in southern Illinois, USA were examined using align with their invasive nature and not with their life integral projection models (IPMs) to determine whether histories. Furthermore, this study demonstrates that more vital rates reflect life history among these closely related research on the competitive nature of Achyranthes species. Two of the species, Amaranthus palmeri and japonica is needed. Amaranthus tuberculatus,aresummerannualsandcon- sidered to be some of the most problematic agricultural Keywords Amaranthaceae Demography Exotic Á Á weeds in the US Midwest. Achyranthes japonica is a species Invasive species Matrix modeling relatively new invasive exotic species that primarily Á Á inhabits forests. Iresine rhizomatosa,isanendangered species in the study area, which also inhabits forests. Two Introduction populations of each species were studied from 2012 to 2014 in which height of individuals were measured and The population dynamics of invasive species differs from used as the state variable in the IPMs. The Amaranthus that of endangered species. Some common characteristics species and Achyranthes japonica had an estimated pop- that invasive species have include: broad-niched, self or ulation growth rate[1, projecting increases in population wind pollination or non-specialized pollinators, rapid size. By contrast, k was \1forI. rhizomatosa,projecting growth to reproductive maturity, high allocation of adeclineinpopulationsizedemonstratingitsendangered resources to reproduction, ability to spread rapidly, prolific status. Germination rates and seed viability were depen- vegetative reproduction, an ability to outcompete native dent on species and varied over time. Elasticity analyses species, and a rapid response to resource availability showed that survival and growth contributed most to k for (Baker 1965; Bazzaz 1986; Simberloff et al. 1997; Sutherland 2004). Few invasive species possess all or most of these characteristics. Possession of these characteristics, Electronic supplementary material The online version of this however, does not necessarily mean that a plant will article (doi:10.1007/s10144-016-0537-2) contains supplementary material, which is available to authorized users. become invasive (Sakai et al. 2001). By contrast, rare and endangered species may exhibit life history characteristics & Lauren M. Schwartz associated with low fitness (Vitousek et al. 1996; Sakai [email protected] et al. 2001). 1 Department of Plant Biology, Center for Ecology, Southern Demographic processes, such as survival, growth, and Illinois University, Carbondale, IL 62901-6509, USA reproduction, can inform us about invasion risk, extinc- 2 Department of Botany and Plant Pathology, Purdue tion risk, and trade-offs in life history strategies. University, West Lafayette, IN 47907, USA Demography links the processes that affect individuals to

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Popul Ecol population and community level patterns (Merow et al. Materials and methods 2014). The diversity of life history characteristics associated with a species are the result of long evolutionary Study sites responses to natural selection over large scales. Studies of closely related species, such as species in the same family, Demographic observations were made at two sites per may be informative in this respect (Boutin and Harper species across southern Illinois. The sites were located 1991). within 145 km of each other (Table 1). Variation occurred The Amaranthaceae family contains important agri- in environmental factors over the three-year study. In 2012, cultural weeds, invasive exotics, and rare native plants. southern Illinois underwent a drought in which over the In the United States Midwest region, Amaranthus pal- growing season (May–October) only 3.3 cm of rainfall meri (S.) Watson and Amaranthus tuberculatus (Moq.) occurred; whereas in 2013 and 2014, southern Illinois Sauer have been widely established as two of the received 9.1 cm and 9.9 cm, respectively, of rainfall (Na- prominent agricultural weeds. These species have many tional Weather Service records). In addition to the drought characteristics that make them very successful weeds year that was experienced in 2012, there were also slightly including the ability to grow 2–3 m in height (Horak higher mean temperatures in 2012 compared with 2013 and and Loughin 2000;TruccoandTranel2011)and 2014. The mean growing season temperature in 2012 was extended seed germination and seedling emergence late 24 °C; whereas in 2013 and 2014, the mean growing sea- into the row-crop growing season (Hartzler et al. 1999). son temperature was 22 °C both years. Achyranthes japonica (Miq.) Nakai is a relatively recent introduction spreading across the Ohio River Valley. Field methods This perennial, C3 herb is native to Korea, China and Japan (Sage et al. 2007;Choietal.2010;Evansand The two populations were monitored for three consecutive Taylor 2011;Schwartzetal.2016). Achyranthes years (2012–2014) at each site. Within each population, ten japonica is generally found in areas with some shade 1-m2 plots were established randomly in sites where the and moist soil. However, the species can also grow in species was known to be present in April 2012. Populations drier areas in sun, and in densely shaded areas of each species were pooled in an area of 200 m2. Overall (Schwartz 2014). Dense patches of Achyranthes japon- in 2012, we found, on average, 1334 individuals of ica have been found in bottomland forests, riverbanks, Achyranthes japonica (density: 35 ± 4 individuals/m2), field edges, and in ditches and swales (Evans and 9564 individuals of Amaranthus palmeri (density: 77 ± 6 Taylor 2011;Schwartz2014;Schwartzetal.2016). individuals/m2), 11,002 individuals of Amaranthus tuber- Apart from anecdotal observations, little has been culatus (density: 106 ± 11 individuals/m2), and 928 indi- reported on this species and only recently has an viduals of I. rhizomatosa (density: 9 ± 2 individuals/m2). aggressive educational campaign been launched to learn The density of individuals per m2 was 29 ± 4 for more about this species. Iresine rhizomatosa Standl. is Achyranthes japonica, 61 ± 5 for Amaranthus palmeri, classified as endangered in Illinois and Maryland and is 92 ± 9 for Amaranthus tuberculatus,5± 1 for I. rhi- considered to be rare in Indiana (IDNR 1994;Gibson zomatosa the following year. and Schwartz 2014). Despite its endangered and rare Seedlings were tagged and monitored by taking node status, very little ecological work has been conducted counts every week throughout each growing season to on this species (Gibson and Schwartz 2014). determine plant size and the following years where appli- We conducted a demographic study to examine the cable (i.e., the perennial Achyranthes japonica and I. rhi- population dynamics of four closely related species to zomatosa). Height measurements were taken at the various determine which vital rate(s) contributed most to popula- stages and used as the state variable. Adult plants were tion growth rate to further understand whether the invasive further classified into reproductive and non-reproductive status or the life history of a species is the driving force plants. Individuals were followed for 3 years or until death. between the closely related species. We analyzed the Demographic parameters were measured each year weekly population dynamics of each species from 2012 to 2014 from May to October. The difference in field season length using integral projection models (IPMs). The objective of depended on weather conditions and seedlings were mon- this study was to evaluate the demographic patterns of each itored as soon as they emerged until after the first frost date of the four species using an IPM to compare vital rates. The of that year. hypothesis was that the invasion status and not the life Flowering was recorded in October of each year: each histories of the species would drive the demographic pro- plant was measured in terms of plant height, number of cesses among these species. nodes and stems as well as the inflorescence length and

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Popul Ecol

Table 1 Site characteristics for each species Species Site name Location Soil typea Land cover Mean Mean temperature precipitation (°C)b (cm)b

Achyranthes japonica Chestnut Hills 37°110N 89°030W Menfro silt loam Forest 22.9 7.5

Achyranthes japonica Cypress Creek 37°170N 89°060W Wheeling silt loam Forest 22.9 7.5

Amaranthus palmeri BRC: 9B 38°300N 89°500W Bethalto silt loam Agriculture ﬁeld 24.5 8.6

Amaranthus palmeri Rend Lake 38°070N 88°540W Wynoose silt loam Agriculture ﬁeld 23.4 7.2

Amaranthus tuberculatus BRC: T4 38°310N 89°500W Bethalto silt loam Agriculture ﬁeld 24.5 8.6

Amaranthus tuberculatus DeSoto 37°470N 89°150W Hurst silt loam Agriculture ﬁeld 23.5 7.3

Iresine rhizomatosa Beall Woods 1 38°200N 87°490W Birds silt loam Forest 23.9 8.3

Iresine rhizomatosa Beall Woods 2 38°210N 87°500W Birds silt loam Forest 23.9 8.3 Data pooled over years a Source: USDA Soil Survey (2015) b Source: National Weather Service (2015) number of inflorescences. Seed number per plant was size were calculated, then model selection methods based determined by cleaning the seed to remove any chaff, then on the Akaike Information Criterion (AIC) were used to counting ten lots of 1000 seeds per sample per site per determine which provided the best fit to the data. Finally, species (i.e., a total of 10,000 seeds per site which is for the analyses, we determined the population growth rate equivalent to 20,000 seeds per species), and finally (k), the P and F (Table 2) kernels, and the elasticity weighing the entire sample. The ten lots of 1000 seeds analysis. For all years, the survival function s(z) was esti- were averaged to determine the final seed count. mated by logistic regression of survival on size z (Fig. 1). Seed viability and germination tests were conducted for Additionally, the mean number of offspring were estimated each species at each site annually. To determine seed from the germination trials (see ESM) and was fitted using viability, seed bags containing 100 seeds each were buried a Poisson linear regression on adult size (P \ 0.05 for all in all plots, just below the soil surface at the end of each years, Fig. 2). Models were fitted using the R package growing season and were retrieved at the beginning of the IPMpack (Metcalf et al. 2013), and the significance of following growing season (Electronic Supplementary nonlinear terms was tested using an ANOVA function with Material (ESM)). Germination tests were performed by a v2 test statistic (Metcalf et al. 2013). Additionally, year hand seeding 10,000 seeds onto the soil surface in ten 1-m2 effects were included in the model, but not site effects plots for each field population in the fall and counting the since preliminary analyses indicated that there was no number that germinated the following spring. The germi- significant difference among sites between species. The nation experiments resulted in an average germination rate P and F kernels are shown separately (Fig. 3) and not as of 86 ± 4.2 % for Achyranthes japonica, 12 ± 2.8 % for the full K kernel because the scales were so different and it Amaranthus palmeri, 14 ± 2.2 % seeds for Amaranthus was difficult to visualize together when the full kernel was tuberculatus, and less than 1 ± 0.3 % for I. rhizomatosa implemented. Seasonal kernels were built, but there was no (Table 2). difference in the trends between the seasonal and pooled data kernels. Thus, the pooled kernels are shown. Data analysis

The implementation of IPMs requires calculating the Results integrals, which is most practically conducted by applying ﬁne categorization (Crawley 2013; Metcalf et al. 2013). The population growth rates (k) for Achyranthes japonica, The limits of integration were determined from the vari- Amaranthus palmeri, and Amaranthus tuberculatus were ance of growth (described in Easterling et al. 2000). The all close to or greater than one for each census period maximum and minimum limits of integration was set by (Table 3). These values of k indicate that the populations adding or subtracting three standard deviations of the were growing. By contrast, Iresine rhizomatosa, however, growth increment based on the maximum and minimum had k values less than one (2012: 0.53; 2013: 0.68) over observed sizes. Alternative statistical relationships for both annual transitions indicating that the populations were growth, survivorship, and fecundity as functions of plant in decline.

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Table 2 Mean fecundity of Achyranthes japonica, Amaranthus palmeri, Amaranthus tuberculatus, and Iresine rhizomatosa Mean seeds/plant Mean germination rate Probability of Seedling—Juvenile Juvenile—Adult Seed viability

Achyranthes japonica 331 0.86 0.67 0.72 0.93 Amaranthus palmeri 15,880 0.12 0.55 0.80 0.64 Amaranthus tuberculatus 63,441 0.14 0.48 0.77 0.71 Iresine rhizomatosa 1000 0.01 0.31 0.45 0.23 Measurements were averaged from 2012 to 2014 and pooled over sites per species. Overall, n = 300 plants/site (i.e., 2012 n = 50 plants/site, 2013 n = 100 plants/site, 2014 n = 150 plants/site)

Fig. 1 Fitting of survival function based upon 2013–2014 data for observed values and the lines represent the ﬁtted values. The ﬁtted a Achyranthes japonica, b Amaranthus palmeri, c Amaranthus curve for each panel is as follows: a log(s/(1 - s)) = 1.23 ? tuberculatus and, d Iresine rhizomatosa grouped over two sites per 0.0156x (P \ 0.05), b log(s/(1 - s)) = 0.23 ? 0.044x (P \ 0.05), species. The survival data are plotted (y-axis: 0 = death; 1 = sur- c log(s/(1 - s)) = 1.06 ? 0.0267x (P \ 0.05), d log(s/(1 - s)) = vival) as a function of individual size x (plant height in cm). The 0.52 ? 0.0012x (P \ 0.05) x-axis scales are different among the panels. The dots represent the

The P kernel for Achyranthes japonica shows that size highest survivorship probabilities (Fig. 3d). Juvenile plants at t ? 1 is not related to size at t, meaning that the small seem to have the lowest survivorship. The Amaranthus plants are expected to grow a lot and the large plants species, however, can reproduce over a wide range of plant shrunk (Fig. 3a). The two Amaranthus species again sizes; whereas, I. rhizomatosa needs to be large in size to showed a similar result in that survivorship increased with reproduce. the growth of the plant (i.e., larger plants had a high sur- In this study, the survival/growth functions made a vivorship) (Fig. 3b, c). The endangered I. rhizomatosa had greater contribution to k than the fecundity function. The a similar P kernel to Achyranthes japonica in terms of elasticity values varied among species and the Amaranthus relatively little growth that occured from 1 year to the next species showed similar results (Fig. 4). Achyranthes and that large-sized reproductive individuals had the japonica and the Amaranthus species had higher values,

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Fig. 2 Number of offspring as a function of individual size [plant a y = 85.77 ? 0.6861x (R2 = 0.609), b y = 4.45 ? 0.0026x (R2 = height (cm)], along with the fitted linear regression for the mean 0.247), c y = 48,000 ? 0.0012x (R2 = 0.027), d y = 0.143 ? number of offspring for a Achyranthes japonica, b Amaranthus 0.0197x (R2 = 0.157). The x- and y-axis scales are different among palmeri, c Amaranthus tuberculatus, and d Iresine rhizomatosa. Data the panels. The dots represent the observed values and the lines pooled over years. The fitted line for each panel is as follows: represent the fitted values

than I. rhizomatosa, for the growth and survival transitions populations of the invasive species, which corresponds of small and intermediate-sized individuals. Iresine rhi- with several other studies (especially in agriculture) (Horak zomatosa, however, had high elasticity values for the and Loughin 2000; Zimdahl 2004; Trucco and Tranel growth and survival transitions of largest sized individuals 2011). This early growth stage is imperative to the survival had the best chance of survival compared with small, of the endangered species as well. Understanding the young individuals. The elasticity values are shown for only dynamics of these species individually can only enhance 2013–2014 because the pattern was similar the prior year. our knowledge when comparing species within a family and projecting the rate of population growth. This knowledge allows land managers to be pre-warned about life- Discussion stage sensitivity of a potential new invasive species coming into an area. Thus, this knowledge allows some time to The four closely related Amaranthaceae species showed develop an appropriate management plan. similar IPM outputs related to life cycle or invasiveness. There were however, differences in seedling density, The two perennial species both had similar P and F kernels survivorship, and fecundity between species and years. showing that the largest plants were the drivers of survival. This response could be due, in part, to varying environ- The annual weedy Amaranthus species and the perennial mental factors. In 2012, southern Illinois underwent a Achyranthes japonica, the invasive species, were similar in drought in which over the growing season (May–October) survival from time t to time t ? 1 and in fecundity, only 3.3 cm of rainfall occurred; whereas in 2013 and although they differ in their life histories. The similarities 2014, southern Illinois received 9.1 and 9.9 cm, respec- between the invasive species and the annual life forms tively (National Weather Service 2015). In addition to the provide insight into management and conservation efforts. drought year that was experienced in 2012, there were also According to our results, the small-sized to intermediate- higher mean temperatures in 2012 compared with 2013 and sized individuals are the most critical for controlling 2014. The mean growing season temperature in 2012 was

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Fig. 3 The P (left panel) and F (right panel) kernels for a Achyranthes japonica, b Amaranthus palmeri, c Amaranthus tuberculatus, and d Iresine rhizomatosa from 2013 to 2014. The lighter areas indicate the more likelihood of transition

24 °C; whereas in 2013 and 2014, the mean growing sea- environmental stress (Grime 1979). Temperature is an son temperature was 22 °C both years. The small indi- important ecological factor in determining species growth viduals were susceptible to drought, especially for I. and productivity. For example Amaranthus palmeri and rhizomatosa. Thus, reallocation of plant resources for Amaranthus tuberculatus exhibit their highest germination survival, in terms of vegetative and root growth, rather than rate of 30 and 50 %, respectively, when mean air temper- fecundity likely occurred during these periods of atures are at 25 °C (Guo and Al-Khatib 2003).

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Table 3 Lambda values (k) for the period 2012–2014 for all species a k 2012–2013 2013–2014

Achyranthes japonica 1.37 1.79 Amaranthus palmeri 1.15 1.22 Amaranthus tuberculatus 0.97 1.18 Iresine rhizomatosa 0.53 0.68 Pooled over sites. Overall, n = 300 plants/site (i.e., 2012 n = 50 plants/site, 2013 n = 100 plants/site, 2014 n = 150 plants/site)

Fig. 4 Elasticity surfaces for the integral projection model ﬁttedc b a Achyranthes japonica, b Amaranthus palmeri, c Amaranthus tuberculatus, and d Iresine rhizomatosa from 2013 to 2014. The x- and y-axis scales [plant height (cm)] are different among the panels. The lighter areas indicate the importance of reproduction and transitions of individuals into the reproductive size classes (the smaller size in year t ? 1 than in year t indicates production of offspring) to k

Habitat type and management strongly influences plant performance (Schwartz et al. 2016). Although causes of mortality were not recorded, disturbances such as flooding, herbicide drift, herbivory, and general human traffic resulted in high mortality of individuals at some sites. c Furthermore, the endangered status of I. rhizomatosa is enhanced by anthropogenic disturbances. These types of disturbances have also increased seedling mortality for other endangered species, such as Mammillaria gaumeri (Britton & Rose) Orcutt, by altering the composition of the surrounding plant community and fragmenting its already restricted habitat (Ferrer-Cervantes et al. 2012). The population growth rate for three of the study species was greater than one, which was expected for agricultural weeds and an invasive species. Lower lambdas (k), as seen in the I. rhizomatosa populations, during some years can be attributed partially to the higher mortality of individuals in those years, which relates to its endangered status. For d example, in 2012, there was a higher mortality, than in other years, for all species due to the extreme drought in southern Illinois. In the following years, the population remained more stable than in the previous year. Elasticity analysis on the whole IPM kernel includes survival, growth, and reproduction and has been used to separate these demographic functions to k from different size classes (Easterling et al. 2000). In general, the vital rates are affected by k the most due to the larger proportion of the stable stage distribution. However, this is altered by the assumption that smaller plants contribute almost no recruits to the next generation (Childs et al. 2004). The elasticity values in this study show that population growth

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Popul Ecol of I. rhizomatosa and the Amaranthus species depends Ferrer-Cervantes ME, Meńdez-Gonza´les ME, Quintana-Ascencio PF, strongly on the retention and survival of larger individuals; Dorantes A, Dzib G, Durań R (2012) Population dynamics of the cactus Mammillaria gaumeri: an integral projection model whereas, growth of Achyranthes japonica populations are approach. Popul Ecol 54:321–334 affected most by demography of smaller individuals. Our Gibson DJ, Schwartz LM (2014) Population dynamics of endangered current knowledge of Achyranthes japonica and I. rhi- Iresine rhizomatosa (Juda’s bush). Grant Agreement No.: zomatosa demography is limited to two sites with different 13-026W Final Report to Illinois Department of Natural Resources. http://opensiuc.lib.siu.edu/cgi/viewcontent.cgi?arti data on growth, survival, and fecundity (Gibson and cle=1004&context=pb_reports. Accessed 20 March 2014 Schwartz 2014; Schwartz et al. 2016). There continues to Grime JP (1979) Plant strategies and vegetation processes. John be a need to more widely measure and model the demog- Wiley & Sons, New York raphy of these closely related species to make generaliza- Guo P, Al-Khatib K (2003) Temperature effects on germination and growth of redroot pigweed (Amaranthus retroflexus), Palmer tions about vital rates. amaranth (A. palmeri), and common tall waterhemp (A. rudis). As this study demonstrates, the invasive nature of a Weed Sci 51:869–875 species and not its life history is a driving factor of pop- Hartzler RG, Buhler DD, Stoltenberg DE (1999) Emergence charac- ulation growth rate. Furthermore, this study provides teristics of four annual weed species. Weed Sci 47:578–584 Horak MJ, Loughin TM (2000) Growth analysis of four Amaranthus insight into the population dynamics of four closely related species. Weed Sci 48:347–355 species in which two of the species are poorly studied. IDNR (Illinois Department of Energy and Natural Resources) (1994) More research is needed on the population dynamics of The changing Illinois environment: Critical trends. Summary these species and how these closely related species interact Report and Volumes 1-7 Technical Report. Illinois Department of Energy and Natural Resources, Springfield, Illinois with one another. Using more sites across different states Merow C, Latimer AM, Wilson AM, McMahon SM, Rebelo AG, would greatly add to what little information is known about Silander JA Jr (2014) On using integral projection models to the population dynamics of these species, especially generate demographically driven predictions of species’ distri- Achyranthes japonica and I. rhizomatosa. butions: development and validation using sparse data. Ecogra- phy 37:1167–1183 Metcalf CJE, McMahon SM, Salguero-Go´mez R, Jongejans E (2013) Acknowledgments We would like to thank Southern Illinois IPMpack: an R package for integral projection models. Methods University Carbondale and the Departments of Plant Biology and Ecol Evol 4:195–200 Plant Soil and Agricultural Systems for their support, Julie Young and National Weather Service (2015) National weather forecast office: Joseph Matthews for help with general organization, several under- Paducah, KY. http://www.weather.gov/climate/index.php?wfo= graduate assistants helped to collect and process samples, and Maria pah. Accessed 7 Jan 2015 Paniw for editing early versions of this manuscript. In addition, we Sage RF, Sage TL, Pearcy RW, Borsch T (2007) The taxonomic would like to thank the Max Planck Institute for Demographic distribution of C4 Photosynthesis in Amaranthaceae sensu Research for teaching us the foundations of IPMs and the Illinois stricto. Am J Bot 94:1992–2003 Department of Natural Resources for providing funding (Grant Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Agreement No.: 13-026W) to work with I. rhizomatosa. Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332 References Schwartz LM (2014) Japanese chaff flower: a rising threat to southern Illinois. River to river cooperative weed management area. Baker HG (1965) Characteristics and modes of origin of weeds. In: http://rtrcwma.blogspot.com/2014/05/japanesechaff-flower-ris Baker HG, Stebbins GL (eds) The genetics of colonizing species. ing-threat-to.html. Accessed 1 May 2015 Academic Press, New York, pp 147–172 Schwartz LM, Gibson DJ, Young BG (2016) Life history of Bazzaz FA (1986) Life history of colonizing plants. In: Mooney HA, Achyranthes japonica (Amaranthaceae): an invasive species in Drake JA (eds) Ecology of biological invasions of North southern Illinois. J Torrey Bot Soc. doi:10.3159/TORREY-D-14- America and Hawaii. Springer-Verlag, New York, pp 96–108 00014 Boutin C, Harper JL (1991) A comparative study of the population Simberloff D, Schmitz DC, Brown TC (1997) Strangers in paradise: dynamics of five species of Veronica in natural habitats. J Ecol impact and management of non-indigenous species in Florida. 79:199–221 Island Press, Washington D.C Childs DZ, Rees M, Rose KE, Grubb PJ, Ellner SP (2004) Evolution Sutherland S (2004) What makes a weed a weed: life history traits of of size-dependent flowering in a variable environment: con- native and exotic plants in the USA. Oecologia 141:24–39 struction and analysis of a stochastic integral projection model. Trucco F, Tranel PJ (2011) Amaranthus. In: Kole C (ed) Wild crop Proc R Soc Lond B 271:425–434 relatives: genomic and breeding resources. Springer-Verlag, Choi CY, Nam HY, Chae HY (2010) Exotic seeds on the feathers of Berlin, pp 11–21 migratory birds on a stopover island in Korea. J Ecol Field Biol USDA Soil Survey (2015) Soil survey. United States Department of 33:19–22 Agriculture: natural resources conservation service. http:// Crawley MJ (2013) The R book, 2nd edn. Wiley, UK websoilsurvey.sc.egov.usda.gov/App/WebSoilSurvey.aspx. Easterling MR, Sp Ellner, Dixon PM (2000) Size-specific sensitivity: Accessed 18 Feb 2015 applying a new structured population model. Ecology Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological 81:694–708 invasions as global environmental change. Am Sci 84:468–478 Evans C, Taylor DD (2011) New invader profile: Japanese chaff Zimdahl RL (2004) Weed-crop competition: a review. Blackwell flower Achyranthes japonica. Wildland Weeds Summer/Fall:4–6 Publishing, Ames

123 Life history of Achyranthes japonica (Amaranthaceae): an invasive species in southern Illinois Author(s): Lauren M. Schwartz, David J. Gibson, and Bryan G. Young Source: The Journal of the Torrey Botanical Society, 143(2):93-102. Published By: Torrey Botanical Society DOI: http://dx.doi.org/10.3159/TORREY-D-14-00014 URL: http://www.bioone.org/doi/full/10.3159/TORREY-D-14-00014

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Life history of Achyranthes japonica (Amaranthaceae): an invasive species in southern Illinois1

Lauren M. Schwartz2, David J. Gibson3, and Bryan G. Young4 Department of Plant Biology, Center for Ecology, Southern Illinois University, Carbondale, IL 62901-6509

Abstract. Achyranthes japonica (Miq.) Nakai (Japanese chaff flower) is a relatively new, invasive species to the United States, with limited information on its life history characteristics. The purpose of this study was to assess the importance of seed survivorship in the soil of A. japonica and to compare survivorship, fecundity, and morphological characteristics within populations at two different sites, Chestnut Hills Nature Preserve (CH) and Bellrose Waterfowl Reserve (BWR), in southern Illinois. Plots were established at each site to determine seed viability by burying seed bags over each of three winters (2012 to 2014) to quantify seedling emergence in the latter 2 yr (2013 and 2014) and to monitor survival of three cohorts of 50 seedlings per site starting in 2012, 2013, and 2014. In addition, 20 reproductive adults were selected outside of the plots to determine average fecundity and to measure a suite of morphological characteristics. Environmental factors had a significant effect on seed viability, which decreased from 2012 to 2013 during a drought year and rebounded from 2013 to 2014 following flooding. On average, individuals at the CH site had higher performance and fecundity when compared with individuals at BWR, regardless of year. Additional differences among the sites, such as dryness, disturbance, and species composition, most likely affected plant performance (i.e. plant height, number of nodes and stems, and inflorescence length). Regardless of high between-population variability, this invasive species has high fecundity, high seed viability, and high propagule pressure that allow rapid spread and expansion of its invasive range. More research is needed on the soil seedbank, seed dormancy, and the effects of stress, which will allow more-informed methods of control. Key words: Achyranthes japonica, invasive species, seedling establishment, seed viability, survivorship

Invasive species are an ever-increasing threat to determined by these demographic processes. natural plant communities (Simberloff et al. The diversity of life history characteristics associ- 2005). In Illinois, nonnative species make up ated with a species is the result of long evolution- about 33.6% of the flora, and many of those are ary responses to natural selection over large invasive, posing a serious threat to natural areas scales (Merow et al.2014).Thus,understanding (Mohlenbrock 2014). Demographic processes, the life history characteristics of invasive species such as survival, growth, and reproduction, can is fundamental for land managers to develop inform us about potential invasion risks, extinc- management and control methods (Meyers and tion risks of native species, and trade-offs in life Bazley 2003). Japanese chaff flower, Achyranthes japonica history strategies. Long-term dynamics of plant (Miq.) Nakai (Amaranthaceae) is an exotic invasions and their effects on the surrounding na- species, originally from Japan, Korea, and tive plant community and ecosystem may be China (Jussien 2014), which is relatively new to North America, where it was first discovered 1 Support was provided by Southern Illinois Uni- in 1981 in Martin County, KY (Medley et al. versity, Carbondale, and by the Department of Plant, 1985). Since then, this species has been found Soil, and Agricultural Systems, specifically the Weed in virtually every county along the Ohio River Science Laboratory, and by the Department of Plant down to the Mississippi River confluence and Biology. Julie Young and Joseph Matthews provided has been spreading up the Ohio River’s comments on manuscript revisions. Several under- graduate assistants helped to collect and process tributaries. By 2015, this species had been con- samples. firmed in nine states (West Virginia, Tennessee, 2 Author for correspondence: [email protected] Kentucky, Indiana, Ohio, Illinois, Missouri, 3 Current Address: Department of Plant Biology, Alabama, and Georgia) and more than 50 Center for Ecology, Southern Illinois University, counties (EDDmapS 2015). The actual distri- Carbondale, IL 62901-6509. 4 Current address: Department of Botany and bution of A. japonica is most likely much great- Plant Pathology, Purdue University, Lafayette, IN er. The lack of public awareness limits 47907. knowledge of this species distribution. The pri- doi: 10.3159/TORREY-D-14-00014 mary mode of dispersal is through water and ECopyright 2016 by The Torrey Botanical Society Received for publication September 13, 2014, and animals (L.M.S., personal observation). in revised form July 6, 2015, and first published Management tactics are lacking for A. japon- March 24, 2016. ica primarily because of poor public awareness

93 94 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143 and the lack of literature on this relatively new continue to develop flowers into the early fall. invader. In addition, few ecological studies Flowers can still form when the seeds mature have been conducted on A. japonica. Many of in the mid to late fall (Schwartz et al. 2015). the ecological studies on A. japonica in the Plants typically die off in the late fall or early United States have been strictly observational winter, but the dead plant stand can remain (Medley et al. 1985; Evans and Taylor 2011; erect even into the winter. Dense populations Schwartz et al. 2015) with one quantitative of A. japonica allow very little to grow under- study (Smith 2013), to our knowledge. Previous neath them (L.M.S., personal observation) dis- studies outside the United States have reported placing native plant species. the dispersal of A. japonica seeds by migratory birds on Korean islands (Choi et al. 2010) and EXPERIMENT SITES. The primary focus of this allelopathic and antimicrobial properties (Kim study was on two abundant populations of 1993, Kim et al. 2004). A. japonica at the Bellrose Waterfowl Reserve The overall objective of this research was to (BWR) in Union County, IL, and Chestnut assess the importance of seed survivorship in Hills Nature Preserve (CH) in Pulaski County, the soil for A. japonica and to compare survi- IL. Both sites have some plant species in com- vorship, fecundity, and performance measure- mon but differ in habitat type. The BWR is ments between populations at two different considered a bottomland hardwood forest or sites in southern Illinois. wetland and the CH is an upland forest that is located near the Ohio River and receives

Materials and Methods. STUDY SPECIES. some flooding in lowland areas. Achyranthes japonica is a perennial, herbaceous The BWR (37u179N, 89u069W) site is a part species that can grow up to 3 m tall. This spe- of the Cypress Creek National Wildlife Refuge cies becomes established as a perennial, capable found within the Cache River wetlands system. of regrowth, at an early growth stage (three The population studied was within 15 m of the or four nodes) (Smith 2013). The leaves of banks of the Cache River (Smith 2013). This A. japonica are opposite and simple. The stem site was historically bottomland hardwood for- is at ground level, and the nodes have a reddish est (McLane et al. 2012). Regular flooding hue, which is a characteristic consistent with occurs at BWR, primarily through the winter other members of the Amaranthaceae family. and spring seasons, creating scour on the forest The flowers occur on erect inflorescences at floor and allowing only minimal organic mat- the end of the stems and upper branches (Evans ter accumulation. The soil type is a wheeling and Taylor 2011). The flowers, which have five silt loam (USDA Soil Survey 2015). Hardwood reflexed tepals (Flora of North America 2015) trees, such as Quercus L. spp. (oak) and Acer L. or sepals (sensu Mohlenbrock 2014), occur in spp. (maple), dominate the canopy with a large tight clusters and diverge at nearly right angles. amount of Taxodium distichum (L.) Rich. (bald As the fruits mature, the spikes elongate, and cypress) (McLane et al. 2012, Smith 2013). the fruits lay flat against the inflorescence Dominant, ground layer species found within branches. The fruits have two stiff bracts that the A. japonica population, include Toxicoden- help in dispersal by attaching to various materi- dron radicans (L.) Kuntze (eastern poison ivy), als, such as clothing, hair, and animal feathers Urtica dioica L. (stinging nettle), Tradescantia or fur (Schwartz et al. 2015). Plants browsed L. spp. (spiderwort), and Polygonum hydropi- by deer or damaged by insects will resprout peroides Michx. (swamp smartweed). and overcompensate in growth and seed pro- The CH (37u119N, 89u39W) site is an 86-ha duction (Smith 2013). Achyranthes japonica upland forest (IDNR 1994). This preserve has can be found growing in areas with partial several unique features, which include a rare, sun and moist soils, but it can also grow in eroding, river bluff community and several heavily shaded and dry areas (Evans and Tay- rare plants and animals (i.e. Halesia diptera lor 2011, Schwartz 2014). Populations of this Ellis [two-wing silverbell], Desmognathus fuscus species have been found in various habitats, Conanti. (dusky salamander]), and wintering including bottomland and upland forests, river- bald eagle [Haliaeetus leucocephalus L.]. This banks, agricultural field margins, and roadside upland forest has a Menfro silt loam soil ditches. (USDA Soil Survey 2015). The overstory com- Achyranthes japonica starts growing in late munity is dominated by Fagus grandifolia spring and flowers in the late summer but can Ehrh. (American beech), Quercus rubra L. 2016] SCHWARTZ ET AL.: LIFE HISTORY OF ACHYRANTHES JAPONICA 95

(northern red oak), and Acer saccharum Mar- through November 2 (216 days), whereas the shall (sugar maple), whereas the understory 2013 and 2014 field seasons ran from June 16 community is dominated by A. japonica, T. through October 16 (122 days) and from May radicans, and U. dioica. 23 through September 13 (113 days), respectively. The difference in field season length POPULATIONS AND PLOT ESTABLISHMENT.At depended on weather conditions, and seedlings each site, a population of A. japonica was sam- were monitored as soon as they emerged pled for 3 consecutive yr (2012 to 2014). Within until after the first frost date of that year. each population, 10 plots (1-m2 each) were Sites were monitored weekly until seedlings established in October/November. In addition emerged. to the annually established plots, the previous years’ plots remained for observations (i.e. SEED VIABILITY. Seed bags each containing 2012, 10 plots site−1; 2013, 10 new plots site−1 100 seeds each were buried in all 10 plots, re- + 2012 plots site−1 [n 5 10; total 5 20]; 2014, gardless of seeding, just below the soil surface 10 new plots site−1 + 2012 and 2013 plots at the end of each growing season and were re- site−1 [n 5 20; total 5 30]). Additionally, five trieved at the beginning of the following grow- seedlings per plot (for a total of 50 plants ing season. Seed bags were kept in place in the site−1 yr−1) were tagged and monitored by tak- soil by the wire from a stake-wire flag, which ing node counts every 2 wk throughout each also aided in retrieval of the bags. The retrieved growing season and the following years where seeds were tested for viability using a tetrazoli- applicable. Tagged plants were classified into um test (1% 2,3,5-triphenyl-2H-tetrazolium stage groups based on node counts: 1 to 4 chloride from MP Biomedicals). The seed coats nodes were seedlings, 5 to 7 nodes were and surrounding bracts were removed, and the juveniles, and 8+ nodes were adults. Adult seeds were dampened in a wet paper towel over plants were further classified into reproductive night. The next day, a dissecting pin was used and nonreproductive plants. Mortality was to puncture the seed coat under a dissecting mi- recorded, but the reason for mortality was not croscope. Then, the seeds were placed in a dark determined (i.e. mammal browsing or natural place in a petri dish to soak in the tetrazolium death from environmental conditions). The solution overnight. The following day, the same tagged plants were monitored the follow- seeds were observed under the dissecting micro- ing years. scope to determine viability. Seed viability was based on the amount of dark-purple–stained SEEDLING EMERGENCE. Achyranthes japonica areas, which indicated living tissue. However, occurred in the plots established in 2012. In light-pink areas represented unstained, dead subsequent years, additional plots (same as tissue (Grabe 1970). More than half of an indi- the established plots in “POPULATIONS AND vidual seed had to be stained dark purple for PLOT ESTABLISHMENT”) were seeded in Octo- the seed to be considered living. ber/November to simulate natural seed rain and the overwintering of seeds (i.e. initial mea- PLANT PERFORMANCE. Flowering of A. japon- surements were made in 2012; in the fall of ica was measured each year at each site. Mor- 2012, the plots for 2013 were established and phological characteristics and fecundity of 20 seeded). Seeds were collected from plants at different randomly selected flowering plants each site to use for the seeded treatment plots. outside of plots was recorded each year. Seed Seven of the 10 plots (seeded treatment plots) production was assessed by counting the seeds on the 20 randomly chosen plants. In all years, were each seeded with 1,000 seeds, and the each of the 20 plants was measured and the remaining three plots were not seeded and are height, inflorescence length (cm), and number considered unseeded controls. These unseeded of nodes, stems, and inflorescences were control plots did not previously have the A. recorded. Density of plants per site and year japonica present in the plots. Sites were moni- were determined by counting individuals in tored weekly from March until seedlings five additional randomly selected 1-m2 emerged. The number of seedlings and quadrats. regrowth of plants from previous years were then recorded within each plot every other DATA ANALYSIS. The percentage of seeds that week until after the first frost date of that emerged was estimated from the data in Fig. 1. year. The 2012 field season ran from April 1 Seeded plots at each field site each had 1,000 96 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143

FIG. 1. Emergence of Achyranthes japonica at (a) Chestnut Hills Nature Preserve (CH) in 2013 and 2014, and at (b) Bellrose Waterfowl Reserve (BWR) in 2014. Zero seedlings emerged at BWR in 2013. Mean values with the same letters are not signiﬁcantly different at a 5 0.05. seeds added, whereas no seeds were added to nodes, and number of stems, increasing signifi- unseeded plots. The difference between the cantly from 2012 to 2013 at BWR but not at numbers of seedlings emerging in seeded plots CH. The difference in density between the two vs. unseeded plots represents an estimate of sites over the 3 yr (moderate, moderate, high how many, out of 1,000 added seeds, germinat- at CH vs. moderate, low, high at BWR) may ed and emerged. A two-way mixed model (SAS have driven the differences in plant-size Institute 2003) was used to determine the measurements. effects of site and year on performance mea- Twenty different plants were chosen for fe- surements (plant height, number of nodes, cundity measurements each year. Fecundity number of stems, inflorescence length, and differed among years (Table 1), with an annual number of inflorescences) and seed viability increase regardless of site. There was about and fecundity. Seedling emergence was ana- a five times increase from 2012 to 2014, regard- lyzed using a repeated-measures mixed model less of site. However, the inflorescence number in SAS (Proc Mixed, SAS Institute 2003) to (4.3 6 1.1) and average length (CH: 10.0 6 determine significant differences in site or 1.7 cm; BWR: 13.7 6 3.2 cm) changed little. year. Significance was assessed at P , 0.05. A All these factors increased somewhat from Tukey’s test was used to determine significant 2012 to 2014, and thus, they have a multiplica- differences among means. tive effect on fecundity. Seed viability had a highly significant inter- Results. All of the interactions between A. action between year and site (P 5 0.0021) japonica sites and the variables measured (Table 1). Regardless of site, there was a decline (Table 1) were significant, which indicates in seed viability from 2012 to 2013, followed by that the pattern of change from 2012 to 2014 an increase in 2013 to 2014. Although this pat- at CH differed significantly from the pattern tern in seed viability between sites seems simi- of change in the variables at BWR. Overall, lar, the proportional drop from 2012 to 2013 the density of plants at CH was 53% greater was greater at BWR than CH. Furthermore, than it was at BWR (mean 6 SE; CH: 22.6 6 the rebound in seed viability from 2013 to 3.7 m2; BWR: 12.0 6 2.0 m2). The density of 2014 was also proportionately greater at BWR. plants was extremely low in 2013 at BWR, Seedling emergence showed a highly signifi- when vegetative size measurements (plant cant interaction between seeding treatment height, number of nodes, number of stems) and year at each site (P 5 0.0001) (Table 1; peaked (Table 1). In contrast, density at CH Fig. 1). In unseeded plots at CH, a mean of remained moderate in 2013, and plant size 17.5 6 2.5 seedlings m−2 emerged in 2013 and measurements were similar to, or slightly lower 4.1 6 0.9 seedlings m−2 emerged in 2014. In than, those in 2012. Inflorescence length shows seeded plots, seedling emergence at CH in- a similar pattern to plant height, number of creased from a mean of 20.4 6 2.7 seedlings 2016] SCHWARTZ ET AL.: LIFE HISTORY OF ACHYRANTHES JAPONICA 97

m−2 in 2013 to 52.5 6 5.1 seedlings m−2 in 2014 (Fig. 1a). The BWR site, however, had P , , 0.0063 , 0.0031 , 0.0047 , 0.0013 , 0.0128 , 0.0001 , 0.0021 , 0.0001 no emergence in 2013 and had a mean of 19.3

d.f. −2

F 6 2.7 seedlings m emerge in the seeded plots 5,48.5 5,33.4 5,33.4 5,38.5 5,33.8 5,65.1 5,65.1 5,44.2 in 2014 with 9.7 6 1.4 seedlings m−2 emerging in the unseeded plots (Fig. 1b). End of growing season survivorship of tagged seedlings was much lower at BWR than it was at CH in each of the three cohorts 7.7 a 4.97 32 a 3.35 3 b 8.27 3 ab2 b3.3 a 2.24 2.1 a 1.89 2.23 6 b 4.55 5.19 throughout the 3 yr (Table 2; Fig. 2a). Addi- 6 6 6 6 6 6 6 6 tionally, the highest seedling survival to reproduction was at CH, regardless of the year the seedlings were initially tagged. At both sites, regardless of year, seedlings that survived became reproductive at the end of the growing season. 7.4 a 108.5 8 b 564 1d 17 3a3a3.4 a1.2 bc 10 28 d 10 14.6 7.3 83 6 6 6 6 6 6 6 6 Discussion. A simple, schematic model sum- marizing the seed dynamics of A. japonica was developed based on our observations of seed viability, seedling emergence, seedling survival values are associated with the interaction between site, year, and to reproduction, and plant fecundity from P 5.9 b 109.1 21 c 263 2c 6 3 ab1 c2.8 b0.3 c 11 17 14.5 c 11 4.1 36 both sites (Fig. 3). This model shows that there and 6 6 6 6 6 6 6 6 is a large potential input of A. japonica seeds F

at Chestnut Hills Nature Preserve (CH) and Bellrose Waterfowl Reserve into the seedbank from reproductive plants, but only a small percentage of seedlings ulti- mately emerge from those seeds the following spring (CH: 0.33%; BWR: 0.55%). However, this low emergence of seedlings does not take 6.1 b 84.5 23 a 112 5a 13 3ab1bc3.1 a 10 1.1 b 7 12.1 3a 2.0 67 6 6 6 6 6 6 6 6 into account seed loss, which could be due to seed predation, decay, dissemination, “hitch

Achyranthes japonica hiking” on people or animals, or environmental factors, such as flooding. The longevity of seed in the seedbank is unknown, and research is needed to understand that part of the life his- 4.6 c 89.9 9 b 632 3b 35 2b2b1.2 c1.3 b 10 14.7 18 8 c 5.2 98 tory. This model provides context for the fol- 6 6 6 6 6 6 6 6 CHlowing interpretation BWR of our results from CH and BWR in 2012 to 2014. Our study demonstrates the highly variable nature of A. japonica plant performance within and among sites and between years in southern 3.7 c 57.6 17 c 264 3 bc 18 2b3a0.9 c0.4 bc 8 7b 10 8.0 5.4 54 Illinois. The significant interaction between 6 6 6 6 6 6 6 6 2012 2013 2014sites and 2012 variables measured 2013 indicates 2014 that morphological traits and population dynamics of A. japonica show different patterns of year- to-year change at different sites, even sites ) 151

1 that are in geographic proximity. This varia- − SE morphological and seed characteristics of ) 15

2 tion in performance of this invasive plant had 6 not been demonstrated quantitatively before this study. However, a previous observational

Mean study (Evans and Taylor 2011) reported relatively similar seed viability (almost 100%) and fecundity (16,000 seeds m−2) of A. japonica, al-

Table 1. beit with a higher density of plants (70 plants −2 Plant height (cm) 64.7 (BWR) in southern Illinois onvariable. 20 Different randomly letters selected plants indicate each significant year difference from among 2012 to years 2014. between The sites. Number of nodesNumber of stemsInflorescence length (cm)Number of inflorescencesFecundity (seeds plant Seed viability (%) 7.4 Density of 3.1 plants (m 8 11 m 78 ). Variation in performance can be 98 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143

Table 2. Percentage of Achyranthes japonica seedlings that survived to reproduction (Number of seedlings that survived to flower/Seedling mortality [m−2]) at Chestnut Hills Nature Preserve (CH) and Bellrose Waterfowl Reserve (BWR) in southern Illinois from 2012 to 2014. Fifty seedlings were tagged and monitored at each site for each of the 3 yr.

CH (%) BWR (%) 2012* 2013 2014 2012* 2013 2014 2012+ 62 (31/19) ——52 (26/24) —— 2013 94 (29/2) 96 (48/2) — 65 (17/9) 56 (28/22) — 2014 76 (22/7) 77 (37/11) 100 (50/0) 76 (13/4) 68 (19/9) 60 (30/20) * Indicates the establishment of original cohort of seedlings. + Indicates the year the original cohort was continually monitored.

FIG. 2. Seedling survivorship of Achyranthes japonica at (a) Chestnut Hills Nature Preserve (CH), and at (b) Bellrose Waterfowl Reserve (BWR) in southern Illinois from 2012 to 2014. Fifty seedlings were tagged and monitored at each site for each of the 3 yr. Closed circles 5 2012 cohort of seedlings that were followed through the 2014 ﬁeld season; open circles 5 2013 cohort of seedlings that were followed through the 2014 ﬁeld season; closed triangles 5 2014 cohort of seedlings. 2016] SCHWARTZ ET AL.: LIFE HISTORY OF ACHYRANTHES JAPONICA 99

FIG. 3. Schematic model illustrating seed dynamics of Achyranthes japonica at (a) Chestnut Hills Nature Preserve (CH) and (b) Bellrose Waterfowl Reserve (BWR) from 2012 to 2014. Values are calculated from data presented elsewhere in this article. Seed loss represents the difference between estimated fecundity and the estimated number of seeds in the soil and represents undetermined seed losses, including dispersal off-site via animals and ﬂooding, seed mortality, and incorporation of viable seed into the long-term, permanent seed bank. Survival of nongerminating seeds and recruitment from long-dormant seeds is undetermined and indicated by a question mark (?). partially attributed to environmental factors. survival, rather than fecundity, likely occurred In 2012, southern Illinois underwent a drought during this time (Grime 1979). Several previous in which, over the growing season (May–Octo- studies report variable performance of invasive ber), 33 cm of rainfall occurred, whereas in species related to environmental stress. For ex- 2013 and 2014, southern Illinois received 47 ample, Gibson et al. (2002) showed that the in- cm and 54 cm, respectively, of rainfall (Nation- vasive exotic grass Microstegium vimineum al Weather Service [2015] records, Paducah, (Trin.) A. Camus (Nepalese browntop) had de- KY [64 km from sites]). In addition to the creased fecundity in drought years. Additional- drought year that was experienced in 2012, ly, an experiment on the invasive annual there were also higher mean temperatures in Anthriscus caucalis M. Bieb. (bur chervil), dem- 2012 compared with 2013 and 2014. The onstrated that survival varied among types of mean growing season temperature in 2012 communities that this species was invading be- was 25 uC, whereas, in 2013 and 2014, the cause fecundity of the A. caucalis was lowest mean growing season temperature was 22 uC in grazed sites (a trampling effect) (Wallace both years. Both of these environmental factors and Pranther 2013). likely increased plant stress in 2012, which is Habitat type was another variable that could potentially why fecundity and seedling survi- have influenced plant performance because the vorship were lowest, regardless of site, in BWR population was located within 15 m of 2012, compared with the following years. A di- the banks of the Cache River, which was stag- rect effect of the reduction in fecundity was seen nant with a high risk for flooding. In 2011 in the low seed viability in 2013, which could and 2013, this site was heavily flooded with partly account for the lack of seedling emer- low species diversity and a lot of bare ground gence at BWR in 2013. Also, the young seed- (Smith 2013). Frequent disturbance at BWR lings were susceptible to the 2012 drought. led to compacted soils and bare ground that Thus, reallocation of plant resources for could have depressed A. japonica germination 100 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143 or seedling emergence. The lack of plant com- Schmid (1999) found a type II survivorship petition, however, allowed for greater avail- curve for the perennial invasive species Solida- ability of resources, which, in turn, may have go altissima L. (Canada goldenrod) when allowed existing A. japonica plants to grow tal- determining the transitions between various re- ler at BWR than they did at CH. The BWR productive stages to assess colonization poten- plants had reduced fecundity compared with tial to new habitats by seed. Survivorship in plants at CH, possibly because of lower light 2013 and 2014 appeared to be moving more to- levels and more-frequent environmental (i.e. ward a type I survivorship curve, which indi- flooding, scouring, and compaction) and ani- cates that mortality risk increases as the mal disturbance (i.e. herbivory), but were ex- maximum life span is reached (Gibson 2014). posed to limited anthropogenic disturbance. The constant mortality risk associated with The CH site was located in a forest that had 2012 is more than likely due to the extreme higher species diversity than found at BWR drought that southern Illinois underwent. Early and had limited anthropogenic or environmen- season conditions, in 2013 and 2014, were con- tal disturbance. Because the CH is “land- ducive for seedling survivorship possibly be- locked” by surrounding private land on three cause of a higher amount of precipitation, sides and the Ohio River to the south, it is not than in 2012, and a colder winter, which could easily accessed by the public, and the site is be important for the seeds in the soil seedbank. rarely used. The presence of the state endan- Understanding how the mortality of this spe- gered dusky salamander (Desmognathus fuscus) cies couples with high fecundity, germination, also limits disturbance at CH because the site is and seed viability provides a foundation to in- protected. vestigate the persistence and establishment of Achyranthes japonica has shown the ability A. japonica further. Thus, from our data, we to resprout and overcompensate in areas that can conclude that land managers should prior- are browsed or mowed (Smith 2013, Schwartz itize managing the low-mortality younger et al. 2015), which allows for an increase in plants, which are otherwise less likely to die, seed output. Little information is known about over adult plants. However, if plants reach the A. japonica’s ability to persist in the soil seed- adult stage, they should be managed before be- bank. However, from our study, and from oth- coming reproductive (Gao et al. 2009). Al- er studies conducted on other species in the though percentage of emergence is low, this Amaranthaceae family (McWilliams et al. species compensates for it with very high prop- 1968), it can be hypothesized that, with its large agule pressure and relatively high seed viabili- seed size, A. japonica seeds may not persist in ty. Populations of other successful invasive, the soil as long as smaller-seeded members of exotic species show both different and similar the Amaranthaceae family (Baskin and Baskin patterns to that of A. japonica. For example, 2014). Large-seeded species may show en- M. vimineum had high levels of seedling emer- hanced survival during seedling establishment gence and seed viability in an open sunny compared with small-seeded species (Moles lawn, but in the woods, both were low (Che- and Westoby 2004). Thompson et al. (1993) plick 2010). Nuzzo (1999) reported that Alliaria proposed a method to predict seed persistence petiolata (M. Bieb.) Cavara & Grande (garlic in the soil based on the variance of fruit length, mustard) had high propagule pressure of 48 width and depth, and weight. Accordingly, we m−2 and high germination rate of 94 to 99% examined 50 randomly chosen A. japonica (Baskin and Baskin 1992). Furthermore, prop- fruits (25 from each site) and determined agule pressure has consistently been highly a mean weight of 126 mg and a total variance correlated with invasion success (Colautti of 0.207 (L.M.S., unpublished data), implying et al. 2006). seed persistence in the soil seedbank for less Our study is, to our knowledge, the first to than 5 yr. empirically assess the invasibility of A. japonica Seedling survivorship at both sites in 2012 in general survivorship, fecundity, and perfor- appeared to exhibit a type II survivorship mance measures. Achyranthes japonica has curve, which indicates a constant mortality been the subject of relatively few investigations, risk throughout the life of the cohort (Gibson which justifies further research on the basic life 2014). This type of survivorship curve is typical history characteristics and competitive abilities. for some herbaceous, perennial plant species For example, this study showed that 19% to (Gibson 2014). For example, Meyer and 36% of the viable seeds produced by mature 2016] SCHWARTZ ET AL.: LIFE HISTORY OF ACHYRANTHES JAPONICA 101 plants in a year emerge as seedlings; this leads CHOI, C. Y., H. Y. NAM, AND H. Y. CHAE. 2010. to several additional questions: (a) what hap- Exotic seeds on the feathers of migratory birds on a stopover island in Korea. J. Ecol. Field pens to the remaining seeds, that is, do they Biol. 33: 19–22. persist in the existing seedbank or do they die; COLAUTTI, R. I., I. A. GRIGOROVICH, AND H. J. MAC‐ (b) how long do seeds persist in the soil seed- ISAAC. 2006. Propagule pressure: a null model bank; and (c) how much does anthropogenic for biological invasions. Biol. Invasions 8: 1023–1037. disturbance truly affect this species. Further- [EDDMAPS] EARLY DETECTION &DISTRIBUTION more, because A. japonica’s population behav- MAPPING SYSTEM. 2015. Retrieved August 3, ior varied so much between the two sites we 2015, from University of Georgia Center for Eco- studied, it will be necessary to study A. japonica system Health. ,http://www.eddmaps.org/. EVANS, C. AND D. D. TAYLOR. 2011. New invader at multiple sites to better understand the popu- profile: Japanese chaff flower—Achyranthes lation biology of this species. These additional japonica. Wildland Weeds Summer/Fall: 4–6. sites could include a variation in flooding and FLORA OF NORTH AMERICA. 2015. Achyranthes ja- disturbance. Alternatively, the study could be ponica (Miquel) Nakai. Retrieved February 18, 2015 from Flora of North America. ,http://www. extended at the current sites of this study to in- efloras.org/florataxon.aspx?flora_id=1&taxon_id= clude more environmental variables, such as 242300552.. light level, soil moisture, soil temperature, and GAO, Y., L. TANG, J. Q. WANG, C. H. WANG, Z. S. the correlation of flood events to mortality. LIANG, B. LI, J. K. CHEN, AND B. ZHAO. 2009. Clipping at early florescence is more efficient for Achyranthes japonica is an aggressive inva- controlling the invasive plant Spartina alterni- sive species that quickly spreads and can invade flora. Ecol. Res. 24: 1033–1041. high-quality natural areas. We have already GIBSON, D. J. 2014. Methods in Comparative Plant Population Ecology, 2nd ed. Oxford University seen it invade into the Cache River watershed, Press, Oxford, UK. which is considered the last remaining high- GIBSON, D. J., G. SPYREAS, AND J. BENEDICT. 2002. quality wetland in southern Illinois (Suloway Life history of Microstegium vimineum (Poaceae), and Hubbell 1994). The habitat type (CH: bot- an invasive grass in southern Illinois. J. Torrey Bot. Soc. 129: 207 219. tomland hardwood forest; BWR: wetland) – GRABE, D.F. 1970. Tetrazolium Testing Handbook and the overall site quality (CH: relatively for Agricultural Seeds: Contribution Number 29 undisturbed, greater species diversity; BWR: to the Handbook on Seed Testing. Tetrazolium frequently flooded, lower species diversity) con- Testing Committee of the Association of Official Seed Analysts and US Department of Agricul- tribute to the difference in results between sites. ture, Washington, D.C. Our data suggest that A. japonica can be GRIME, J. P. 1979. Plant Strategies and Vegetation a threat to both habitats but is, potentially, Processes. John Wiley & Sons, New York, NY. a greater threat to the higher species diversity [IDNR] ILLINOIS DEPARTMENT OF ENERGY AND NATU- RAL RESOURCES. 1994. The Changing Illinois En- site than to the more-disturbed site. This con- vironment: Critical Trends—Summary Report clusion is of great concern because invasive spe- and Volumes 1–7 Technical Report. Illinois De- cies usually perform better in more-disturbed partment of Energy and Natural Resources, areas (Jauni et al. 2015). How far this species Springfield, IL. JAUNI, M., S. GRIPENBERG, AND S. RAMULA. 2015. can spread, both geographically and into vari- Non-native plant species benefit from distur- ous habitat types, remains unknown. More bance: a meta-analysis. Oikos 124: 122–129. knowledge is needed on this species to generate JUSSIEN,A.L.2014.Amaranthaceae,Floraof an efficacious management strategy that can be Taiwan. Retrieved December 16, 2014, from South China Botanical Garden,Guangzhou,Guangdong implemented to better control this species in the Province, P. R. China. ,http://www.efloras.org/ future. florataxon.aspx?flora_id=101&taxon_id=10031.. KIM, J. C., G. J. CHOI, S. W. LEE, J. S. KIM, K. Y. Literature Cited CHUNG, AND K. Y. CHO. 2004. Screening extracts of Achyranthes japonica and Rumex crispus for ac- BASKIN, C. C. AND J. M. BASKIN. 1992. Seed germina- tivity against various plant pathogenic fungi and tion biology of the weedy biennial Alliaria petio- control of powdery mildew. Pest. Manag. Sci. lata. Nat. Areas J. 12: 191–197. 60: 803–808. BASKIN, C. C. AND J. M. BASKIN. 2014. Seeds: Ecolo- KIM, K. U. 1993. Integrated management of paddy gy, Biogeography, and Evolution of Dormancy weeds in Korea, with an emphasis on allelopathy. and Germination, 2nd ed. Academic Press, Ox- Food Fertil. Technol. Cent. 2: 8–20. ford, UK. MCLANE,C.R.,L.L.BATTAGLIA,D.J.GIBSON, CHEPLICK, G. P. 2010. Limits to local spatial spread AND J. W. GRONINGER.2012.Successionof in a highly invasive annual grass (Microstegium exotic and native species assemblages across vimineum). Biol. Invasions 12: 1759–1771. achronosequenceofrestoredfloodplainforests: 102 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143

atestoftheparalleldynamicshypothesis.Restor. 2014, from the River to River CWMA. ,http:// Ecol. 20: 202–210. rtrcwma.blogspot.com/2014/05/japanese-chaff- MCWILLIAMS, E. L., R. Q. LANDERS, AND J. P. MAHL- flower-rising-threat-to.html.. STEDE . 1968. Variation in seed weight and germi- SCHWARTZ, L. M., K. M. SMITH, C. EVANS, K. L. nation in populations of Amaranthus retroflexus GAGE, D. J. GIBSON, AND B. G. YOUNG. 2015. L. Ecology (Wash. D. C.). 49:290–296. Fact sheet: ecology and control of Japanese chaff MEDLEY, M. H., H. BRYAN, J. MACGREGOR, AND J. flower [Achyranthes japonica (Miq.) Nakai]. W. THIERET. 1985. Achyranthes japonica (Miq.) Retrieved January 15, 2015, from the River to Nakai (Amaranthaceae) in Kentucky and West River CWMA. ,http://www.rtrcwma.org/Chaff_ Virginia: new to North America. SIDA Contrib. FactSheet.pdf. Bot. [J. Bot. Res. Inst. Tex.]. 11: 92–95. MEROW, C., A. M. LATIMER, A. M. WILSON, S. M. SIMBERLOFF, D., I. M. PARKER, AND P. N. WINDLE. MCMAHON, A. G. REBELO, AND J. A. SILANDER 2005. Introduced species policy, management, JR. 2014. On using integral projection models to and future research needs. Front Ecol Environ. generate demographically driven predictions of 3: 12–20. species’ distributions: development and validation SMITH, K. M. 2013. Invasion and management of using sparse data. Ecography 37: 1–17. Achyranthes japonica in a southern Illinois wet- MEYER, A. H. AND B. SCHMID. 1999. Seed dynamics land. M.S. thesis. Southern Illinois University, and seedling establishment in the invading peren- Carbondale, IL. nial Solidago altissima under different experimen- SULOWAY L. AND M. HUBBELL. 1994. Wetland tal treatments. J. Ecol. 87: 28–41. Resources of Illinois: An Analysis and Atlas— MEYERS, J. H. AND D. R. BAZELY. 2003. Ecology and Special Publication 15. Illinois Natural History Control of Introduced Plants. Cambridge Univer- Survey, Champaign, IL. sity Press, New York, NY. THOMPSON, K., S. R. BAND, AND J. G. HODGSON. MOHLENBROCK, R. H. 2014. Vascular Flora of Illinois: A Field Guide, 4th ed. Southern Illinois 1993. Seed size and shape predict persistence in University Press, Carbondale, IL. soil. Funct. Ecol. 7: 236–241. USDA SOIL SURVEY. 2015. Soil Survey. Natural MOLES, A. T. AND M. WESTOBY. 2004. Seedling survival and seed size: a synthesis of the literature. resources conservation service. Retrieved Febru- J. Ecol. 92: 372–383. ary 18, 2015, from United States Department of NATIONAL WEATHER SERVICE. 2015. National weather Agriculture. ,http://websoilsurvey.sc.egov.usda. forecast office: Paducah, KY. Retrieved July 17, gov/App/WebSoilSurvey.aspx.. 2015 from National Weather Service. ,http:// WALLACE, J. M. AND T. S. PRATHER. 2013. Compara- w2.weather.gov/climate/index.php?wfo=pah.. tive demography of an exotic herbaceous NUZZO, V. 1999. Invasion pattern of the herb garlic annual among plant communities in invaded can- mustard (Alliaria petiolata) in high quality forests. yon grassland: inferences for habitat suitability Bio Invasions 1: 169–179. and population spread. Biol. Invasions 15: SAS INSTITUTE,INC. 2003. SAS 9.1, SAS Institute, 2783–2797. Cary, NC.` WESTMAN, W. E. 1990. Park management of exotic SCHWARTZ, L. M. 2014. Japanese chaff flower: A ris- plant species: problems and issues. Conserv. ing threat to southern Illinois. Retrieved May 28, Biol. 4: 251–259. Schwartz et al. — Competitive nature of four closely related Amaranthaceae species

Introduction Lehman and Tilman 2000). In general, the speciﬁc rate of biomass change of a species is based on the limiting Invasive species have large ecological impacts on native resources in the environment (Tilman 1985; Krueger- species, communities and ecosystems (Elton 1958; Mangold et al. 2006). The growth of a plant would decrease Simberloff et al. 1997; Blackburn et al. 2014). There are in the presence of a neighbouring plant if these plants con- 50 000 invasive species and the number is steadily " sumed the same limiting resources (Tilman 1988, 1997; increasing (Sakai et al. 2001). About 42 % of the species Maron and Marler 2007). While Tilman’s resource ratio on the threatened and endangered species list are at risk model has been widely used in natural systems, it is less primarily because of invasive species (Sakai et al. 2001; widely applied in crop systems although the model still Pimentel et al. 2005). For example, in Illinois, the location applies (Zimdahl 2004; Miller et al. 2005). of this study, 1156 invasive plant species had escaped The Amaranthaceae family contains important agricul- cultivation and became naturalized by 2014, equivalent tural weeds, invasive exotics and rare native plants to 32.1 % of the state’s total ﬂora (Mohlenbrock 2014). providing a useful system to test concepts related to com-

Of that percentage, 78 % of the species were introduced petitiveness among closely related species. In the US Mid- Downloaded from from outside of North America (IDNR 1994). However, west region, Palmer amaranth (Amaranthus palmeri) and predicting whether or not an introduced species will tall waterhemp (Amaranthus tuberculatus) have been become invasive can be difﬁcult although there is a strong acknowledged as two of the most problematic and wide- incentive to determining which plants are likely to become spread agricultural weeds (Bensch et al.2003; Ward et al. invasive before they become too widespread and unman- 2013). These species have many characteristics that make http://aobpla.oxfordjournals.org/ ageable (Westbrooks 2004). them successful weeds, including the ability to grow 2–3 m Different approaches have been advocated to assess in height (Horak and Loughin 2000; Trucco and Tranel 2011), invasive potential. These include examining plant func- aprolongedperiodofseedgerminationandseedlingemer- tional traits, quantifying competitive ability and phylogen- gence late into the row-crop growing season (Hartzler et al. etic comparisons. Of these, ecologists are increasingly 1999). Competition of 8 plants m22,startingatcropemer- relying on plant functional traits as a way to understand gence, resulted in Palmer amaranth reducing soya bean some of the most fundamental and applied questions yields by 78 % compared with 56 % for tall waterhemp because trait-based approaches can help to disentangle

(Bensch et al. 2003). Furthermore, soya bean yield was at Arkansas Multisite on January 21, 2016 the effect of ecological processes on communities (Dıáz reduced by 10 % when plants emerged at the V4 growth et al. 2007; Carmona et al. 2015). Furthermore, testing stage of soya bean (Steckel and Sprague 2004; Steckel these methods are critical because it forms a pathway by et al. 2004, 2008). Palmer amaranth and tall waterhemp which plant functional traits influence community assem- have been found to be very competitive not only with row bly, the outcome of biological invasions and species diver- crops but also with other Amaranthus species (Trucco and sity effects on ecosystem function (McGill et al. 2006; Kraft Tranel 2011). et al. 2015). Some of the literature connects plant func- Japanese chaff flower (Achyranthes japonica) is also in tional traits to competitive outcomes. For example, species the Amaranthaceae and represents a relatively recently may differ in traits that influence their ability to draw down introduced species that is spreading across the Ohio shared limiting resources or produce offspring, and the River Valley (Schwartz et al.2015, 2016). This monoe-

resulting average fitness differences may favour competi- cious, perennial, C3 herb is native to Korea, China and tive exclusion (Tilman 1982; Chesson 2000). Competitive Japan (Sage et al. 2007; Choi et al. 2010; Evans and Taylor ability is further correlated with plant functional traits 2011; Schwartz 2014). Japanese chaff flower is generally (Zhang and Lamb 2012) in each life stage (Wang et al. found in areas with some shade and moist soil. However, 2010). the species can also grow in drier areas in sun and in Competitive ability can be compared between species in densely shaded areas (Schwartz 2014, 2015). Dense two ways: first, by assessing the competitive effect of patches of Japanese chaff flower have been found in plants or the ability to suppress other individuals, and sec- bottomland forests, riverbanks, field edges and in ditches ondly, by assessing the competitive response of plants or and swales (Evans and Taylor 2011; Schwartz 2014; the ability to avoid being suppressed (Goldberg and Schwartz et al.2016). Large patches of Japanese chaff Landa 1991; Violle et al. 2009; Zhang and Lamb 2012). flower have shown indications of deer browsing and Mechanistically, competition can be understood in terms insect feeding, but the plant will release new shoot of Tilman’s resource ratio model that predicts that the growth from previously dormant axillary buds and over- growth rate of an individual is determined by the two compensate (Schwartz et al. 2016). Apart from anecdotal resources at the lowest availability relative to the plant’s observations, little has been reported on this species and requirement for all resources (Tilman 1982, 1987, 1997; only recently has an aggressive research campaign been

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launched to learn more about this species. The occur- flower seed was collected from Chestnut Hills Nature Pre- rence of Japanese chaff flower in row-crop field margins serve (CH: 37811′N, 8983′W) located in Pulaski county, Illi- in southern Illinois has prompted concern about its nois, and bloodleaf seeds were collected from Beall potential competitive effects on crops. In contrast, blood- Woods Nature Preserve (BW: 38820′N, 87849′W). Seeds of leaf (Irisine rhizomatosa) is classified as endangered in the two annual Amaranthus species (Palmer amaranth Illinois and Maryland and is considered to be rare in Indi- (located at the Belleville Research Center (BRC 9B: ana (IDNR 1994; Gibson and Schwartz 2014). Despite its 38830′N, 89850′W)) and tall waterhemp (located at BRC endangered and rare status, very little ecological work T4: 38831′N, 89850′W) were collected from glyphosate sus- has been conducted on this species (Gibson and Schwartz ceptible populations and underwent a bleach (5.25 % 2014). sodium hypochlorite) scarification process to ensure max- In this study, we conducted experiments based on the imum possible seed germination. The soya bean, Japanese above approaches in a multi-year, temporally replicated, chaff flower and bloodleaf seeds did not require pretreat- set of experiments to compare these assessment meth- ment. Seeds of each species were sown into separate ods to determine the invasive potential of Japanese chaff flats with potting soil and allowed to germinate. Seeding Downloaded from flower. We compared plant traits and competitive ability rates and timing were determined based on previously of Japanese chaff flower with two invasive agricultural measured germination rates and establishment times species and one endangered confamilial plant species for each species (e.g. Japanese chaff flower was seeded in the Amaranthaceae. Additionally, we assessed the 10 days before tall waterhemp). When seedlings of each invasive potential based on each of these approaches species had emerged, five seedlings per species were trans- http://aobpla.oxfordjournals.org/ and determined the degree of agreement between planted into each experimental pot. Seedling density was them. Thus, the objective of this study was to determine chosen based on pot size. We did not want the pot size to the relative competitive effect and response of closely be a limitation to plant growth. related species in the same family to a crop. Two hypoth- Field soil (0–15 cm depth) was collected from Southern eses were tested: (1) the perennial species, Japanese Illinois University Agronomy Research Center (ARC). Soil chaff flower and bloodleaf, will have a lower resource was characterized as having a topsoil of silt loam requirement than the annual Amaranthus species when (0–0.25 m) and subsoil (0.25–1.30 m) of silt clay loam

competing with interspecific neighbours (measured as (Herman et al. 1976). Field soil was sterilized and mixed at Arkansas Multisite on January 21, 2016 resource drawdown) and (2) a competitive effect ranking in the ratio of 1 : 1 with sterilized sand to dilute the N con- would be Palmer amaranth . tall waterhemp . cut centration and aid in permeability while watering. The Japanese chaff flower Japanese chaff flower blood- mixed soil was placed into 15-cm pots. The average green- ¼ ¼ leaf. The competitive response rankings will be inversely house conditions included a photoperiod of 8–12 h per " related among the four species. The rationale behind day, which were determined by supplemental lights in the the hypothesized ranking was developed from personal greenhouse, and a temperature of 31 + 5 8C. Two soya observations and a literature review of the species. bean (Asgrow Brand AG3832 plot seed, Illinois origin) seeds were planted in each pot for a density equivalent Methods to soya beans grown in a 38-cm row spacing in agricultural fields. We tested our hypotheses by conducting two experi- Resource manipulation treatments of N addition and ments. A resource drawdown experiment was conducted light reduction (shading) were implemented. Nitrogen to test how each species utilizes an above- and below- was added as granular ammonium nitrate applied at ground resource (test of Hypothesis 1), and a field experi- 1 g per pot prior to transplanting the seedlings. Shading ment was conducted to determine the competitive treatments were implemented by surrounding the pots effect and response of the study species on soya beans with a frame and then covering the frame with a 60 % at varying densities and soya bean row spacing (test of shade cloth to simulate forested or crop canopies. Hypothesis 2). A frame constructed of PVC pipe was placed around the non-shaded pots to control for shade effects produced Resource drawdown experiment by the frames. Pots were watered twice daily with 75 mL. The drawdown of light and soil nitrogen (N) by each species There were five replicates (plus one unseeded control pot) was determined in field soil under greenhouse conditions of each treatment with two temporal replicates. Control at the Southern Illinois University Tree Improvement Center pots were not sown with seeds to establish a baseline for (TIC) greenhouse. Seeds of each of the four Amarantha- resource drawdown values. Each run of the experiment ceae species were collected from populations within lasted 4 weeks. Pots were placed in the greenhouse in " 161 km of Carbondale, Illinois, each year. Japanese chaff a randomized complete block design.

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Data collection. Light intensity drawdown was measured TIC field. The soil was prepared as in the resource under the plants at the soil surface using a LI-COR Light drawdown experiment. The soya bean, Japanese chaff Meter (Model LI-250; LI-COR, Lincoln, NE, USA) for each flower and bloodleaf seeds did not require pretreatment. pot twice per week. Light quality was measured one time However, as in the resource drawdown experiment, the at the end of the experiment using an International Light two Amaranthus species (Palmer amaranth and tall 1400A radiometer/photometer (IL1400A; International waterhemp) were scarified with bleach solution to Light, Inc., Newburyport, MA, USA) using white, blue, red promote germination. After seedling emergence, the (R) and far-red (FR) filters below the leaves. The light seedlings were transferred to the field and the pots were quality meter was placed below a leaf of each plant. submerged into excavated holes, so the soil surface in Light quality was performed on a separate set of pots the field and pots were equivalent. Pots were used to that did not undergo the N or light treatments. prevent the release of Japanese chaff flower into the Performance measurements (height and number of field, since at the time of this experiment this species had nodes) were recorded twice weekly to use as an indicator not been found in Jackson county, Illinois. In addition, the of early seedling growth. Above- and belowground bio- planting of an endangered species such as bloodleaf is Downloaded from mass were harvested from each pot when the seedlings heavily regulated and the pots provided containment. of each species had reached four nodes indicative of Volunteer plant seedlings were removed continually early seedling growth. Thus, all of the plants within a spe- throughout the experiment. Each year (2012–14), the cies were harvested at the same time, but the actual har- experiment was conducted until the plants within a http://aobpla.oxfordjournals.org/ vest date between species varied (i.e. the Amaranthus species reached the end of the seedling stage (denoted species reached the four-node stage before the perennial by the majority of each species reaching the four-node species and were harvested a week earlier). Biomass was stage) to seek consistent results. Thus, each species had oven dried (48 h, 55 8C) and weighed. Inorganic N was one harvest, but the harvest date may have differed measured in the soil of each pot using ion-exchange between species. Plants in this experiment were not resin bags (Binkley 1984). Resin bags were placed into grown beyond the seedling stage because control of the pot the day that the pots were sown and removed agronomic weeds is frequently targeted at this stage. the day that the pots were harvested. Resin bags were con- Each of the four invasive species (n 5 for invasive spe- ¼ structed from nylon hose and consisted of 5 g of equal cies treatment including cut and uncut Japanese chaff at Arkansas Multisite on January 21, 2016 amounts of an anion (Dowex 1 8, 50–100 mesh; Acros × flower, see below) were planted either as a monoculture Organics) and a cation (Dowex 50W 8, 50–100 mesh; (control) or with soya bean (n 2 for soya bean treat- × ¼ Acros Organics) resin. In the laboratory, the resin was ment) (Asgrow Brand AG3832 plot seed, Illinois origin). extracted with 75 mL of 2 N KCl after shaking for 1 h at Japanese chaff flower seedlings were planted either as 200 r.p.m., filtered through a 0.4-mm filter membrane un-manipulated seedlings (referred to as uncut Japanese and the filtrate analysed for NH4-N and NO3-N on a Flow chaff flower, ACHJA) or as seedlings cut back to the soil IV Solution Autoanalyzer (O.I. Corporation, College Station, surface at the four-node stage (cut Japanese chaff flower, TX, USA). Total N was determined by adding the NH4-N and ACHJA-C) at which point seedlings have reached a peren- NO3-N values. nial growth stage (Smith 2013). The cut Japanese chaff flower plants represent perennial plants that may have Seedling competitive effect and response survived the previous winter or regrowth from the applica- experiment tion of a non-systemic herbicide typically applied prior to Study site. Experimental plots were established at the commercial soya bean planting. Upon emergence, the Southern Illinois University, Carbondale TIC in Jackson Amaranthaceae seedlings were thinned down to the County, Illinois (37842′N, 89816′W). The soil at the site was desired seedling densities per pot (10, 30 and 90 for asiltclayloam,withatopsoilofsiltloamandsubsoilofsilt 38-cm rows (Trial 1) and 10 and 30 for 76-cm rows (Trial clay loam (Herman et al. 1976). The experiment was 2)). Each trial was conducted each year. From here forward, conducted annually for 3 years (2012–14), with 2012 the 10 seedlings per pot density will be referred to as low, being a preliminary experiment (data not reported). the 30 seedlings per pot as medium and the 90 seedlings per pot as high density. One or two equidistant soya bean Experimental design. Seeds, which were collected in seedlings were planted 4 cm apart in each pot to simulate southern Illinois that year and were from the same seed typical planting densities of soya bean (Bensch et al. 2003) source as the resource drawdown experiment, were with the Amaranthaceae densities chosen to allow for planted in sterilized pots (15 cm diameter by 15 cm agricultural conditions of crowding and competition depth) filled with a silt clay loam soil collected from the around the soya bean plants. One soya bean per pot

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represented a 76-cm row spacing for soya beans (Trial 2), Results whereas two soya bean per pot represented a 38-cm row spacing (Trial 1). Resource drawdown This experimental design was an additive design with In comparison with the controls (pots with no plants), the repeated measures (Gibson et al. 1999; Gibson 2015). four Amaranthaceae species each drew down light, but The treatment design was a fully factorial combination not N (Fig. 1). In terms of light drawdown, bloodleaf of the four Amaranthaceae species including two stages drew down the least amount of light (which means that of Japanese chaff flower (see below) (n 5), four or bloodleaf would have the highest percentage of light ¼ three different densities (n 4 (38-cm rows) or n 3 available at 69.2 + 5.6 %), indicating that this species ¼ ¼ (76-cm rows)), presence or absence of a soya bean cultivar had the least amount of plant material shading the soil (n 2) and four or three replicates (n 4 (38-cm rows) or surface. Palmer amaranth and soya bean drew down the ¼ ¼ n 3 (76-cm rows)) for a total of 5 4 2 4 160 greatest amount of light (26.8 + 3.5% and 30.2 + 2.8 %, ¼ × × × ¼ experimental units (pots) for the 38-cm rows and 5 respectively), and tall waterhemp and Japanese chaff × 3 2 3 90 experimental units (pots) for the 76-cm flower drew down an intermediate level of light in Downloaded from × × ¼ rows, a grand total of 250 pots (50 pots per species). comparison with the other species (41.4 + 2.9 and 45.6 + 2.2 %, respectively). Data collection. Height (cm), number of branches, nodes There was no significant difference for aboveground bio- and leaves were measured twice a week for each mass between N treatment levels and species, except for individual to determine performance. All seedlings in Japanese chaff flower and Palmer amaranth (Table 1, http://aobpla.oxfordjournals.org/ each pot were harvested when the majority of the Fig. 2A). A significant aboveground biomass interaction individuals had reached the four-node stage, oven dried occurred between species and shading treatment (Fig. 2B). at 55 8C and both above- and belowground biomass Each species produced more aboveground biomass without weighed (g). Light intensity and soil moisture were the shading than under the 60 % shading treatment, except measured twice per week in each pot using a LI-COR bloodleaf. Again, Japanese chaff flower produced a similar

Light Meter (Model LI-250; LI-COR) and ECH2O Decagon amount of aboveground biomass (0.75 + 0.03 g per pot) Soil Moisture meter (Decagon Devices, Inc., Pullman, to both Palmer amaranth (0.6 +0.04 g) and tall waterhemp WA, USA), respectively. (0.55 + 0.02 g) without shading. The soya bean crop pro- at Arkansas Multisite on January 21, 2016 duced the largest aboveground biomass (2.5+ 0.03 g), Statistical analysis whereas bloodleaf produced the smallest biomass For the resource drawdown experiment, a three-way (0.3 + 0.01 g). Belowground biomass was affected by mixed model (SAS Institute) was used to determine the the shade treatment (Table 1), and there was a trend fixed effects of treatment (N, light), density and plant spe- towards an increase for the Amaranthus species and a cies on plant performance (plant height and nodes). Light decrease for Japanese chaff flower and soya bean in quality was analysed using a two-way mixed model test- belowground biomass with additional soil N (Fig. 2C). ing the effects of light wavelength and plant species on light reduction. The competition experiment was analysed using a repeated-measures three-way mixed model in SAS (PROC MIXED, SAS Institute) to detect treatment effects (fixed effect: weed density, soya bean presence or absence and weed species) on the performance (height, branch numbers, nodes and leaf numbers), light intensity and soil moisture. Random effects were blocks of pots in all tests. Aboveground and belowground biomass were analysed for the Amaranthaceae species and soya bean separately using a two-way mixed model to determine the effect of biomass and density or soya bean presence or absence. Significance was assessed at P , 0.05. A Tukey’s test was used to determine significant differences among means with signifi- Figure 1. Relative resource drawdown for total N and light intensity cant treatment effects. Based on weed species and soya at the soil surface for bloodleaf (IRERH), Japanese chaff flower bean performance, a competitive effect and response (ACHJA), Palmer amaranth (AMAPA), tall waterhemp (AMATA), soya ranking was proposed (after Bensch et al. 2003; Zhang bean (GLYMX) and control (C) with 95 % confidence intervals. n 40 ¼ and Lamb 2012). plants/species.

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Table 1. F and P statistics for above- and belowground biomass (g), in the greenhouse experiment, for N and light for the four Amaranthaceae species and soya bean. df, degrees of freedom. 1Treatments with and without the 60 % shade cloth (n 2). 2Treatments with and without the ¼ addition of ammonium nitrate (n 2). 3All study species (n 5). ¼ ¼ Treatment/variable df Aboveground biomass Belowground biomass ...... FP FP ...... Shading1 1, 12 17 ,0.0001 71.35 ,0.0001 Nitrogen2 1, 12 17 ,0.0001 61.05 ,0.0001 Shading nitrogen 4, 64 3.71 0.0864 9.39 0.0069 × Species3 4, 28 59.9 ,0.0001 19.89 ,0.0001 Species shading 4, 64 3.94 0.0064 6.26 0.0003 × Species nitrogen 4, 64 2.19 0.0799 4.12 0.0051 × Downloaded from Species shading nitrogen 4, 64 59.9 0.6753 3.68 0.0092 × × http://aobpla.oxfordjournals.org/ at Arkansas Multisite on January 21, 2016

Figure 2. Mean (+SE) aboveground biomass in response to (A) N and (B) light treatments, and (C) belowground biomass in response to the interaction between N and light treatments. Species nomenclature is as follows: bloodleaf (IRERH), Japanese chaff ﬂower (ACHJA), Palmer amaranth (AMAPA), tall waterhemp (AMATA) and soya bean (GLYMX). *Above pairs of bars indicates a signiﬁcant difference (a 0.05) between mean ¼ values in aboveground biomass comparisons between monocultures with or without N or light.

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the highest density (90 seedlings per pot), both Amar- anthus species reached the same height by the ﬁnal day after planting (DAP) (Fig. 4A). In 2014, however, there was an interaction between species, DAP and soya bean (Table 2). Regardless of the trial, when soya beans were present, the height of bloodleaf was reduced (Fig. 4C and D). By DAP 23 in both trials, monocultures of seedlings of the two Amaranthus species were the largest, with both cut and uncut Japanese chaff ﬂower seedlings only 1 cm shorter. Bloodleaf was the shortest in both trials each year. The competitive response between years, regardless of trial, was comparable with each other.

The competitive effect of the study species on soya Downloaded from Figure 3. Mean (+SE) per cent reduction of light quality in response beans was only apparent in Trial 2 in 2013 (Fig. 5A) and to study species and soya bean. Species nomenclature is as follows: Trial 1 in 2014 (Fig. 5B). There was an interaction between bloodleaf (IRERH), Japanese chaff flower (ACHJA), Palmer amaranth species and density in both trials. In Trial 2 in 2013 (P (AMAPA), tall waterhemp (AMATA) and soya bean (GLYMX). Mean ¼ 0.015), the highest density of cut Japanese chaff flower values with the same letters are not significantly different at http://aobpla.oxfordjournals.org/ a 0.05 within a species. reduced the height of soya bean the most, followed by ¼ the two Amaranthus species, uncut Japanese chaff flower and bloodleaf. For the lowest density, the cut Japanese A greater amount of belowground biomass was attribu- chaff flower again reduced the height of the soya beans ted to the N addition for all species, especially Japanese the most, followed by uncut Japanese chaff flower and chaff flower (2.7 + 0.3 g). Belowground biomass of Palmer amaranth. Although the reduction in height was Palmer amaranth and tall waterhemp were similar relatively small (1.8–3.1 cm), both uncut Japanese chaff regardless of soil N treatment without shading. flower and the cut Japanese chaff flower reduced the An interaction between wavelength and species

height of soya bean in a similar manner to the two Amar- at Arkansas Multisite on January 21, 2016 (P , 0.0001) was evident for the mean reduction in light anthus species with bloodleaf having no effect at all three quality (Fig. 3). Bloodleaf (60.7 + 1.5 %) and soya beans densities. The same trend in soya bean height reduction (57.2 + 2.9 %) had the lowest FR light reduction through across all densities occurred in Trial 1 in 2014: the pres- shading, whereas Japanese chaff flower had the higher ence of tall waterhemp caused the greatest height reduc- reduction (97.3 + 0.5 %). The Amaranthus species had a tion, followed by the cut Japanese chaff flower and uncut similar reduction of FR light (AMAPA: 54.5 + 1.1 %; Japanese chaff flower, with Palmer amaranth reducing AMATA: 52.4 + 2.7 %). All of the species showed a mean the height the least. Consistency in results between trials per cent reduction in R light quality, but Japanese chaff and years supports intrinsic differences among species flower reduced R light the least (57.0 + 1.1 %). In this rather than short-term environmental variability (pheno- study, the R/FR ratios were comparable for all of the spe- typic plasticity). cies (P . 0.05)—bloodleaf: 1.37 + 0.58, Japanese chaff There was an interaction between DAP, density and soya flower: 1.51 + 0.45, Palmer amaranth: 1.51 + 0.64, tall bean (Table 2) affecting soil moisture in 2013. The soil waterhemp: 1.56 + 0.82 and soya bean: 1.43 + 0.56. moisture in the pots with densities of 10, 30 or 90 seedlings per pot was relatively similar regardless of trial [see Competitive effect and response Supporting Information—Fig. S1]. In 2014, however, The competitive response of the study species to soya there was an interaction between DAP and soya bean. bean was similar between trials within the same year. In both trials at DAP 10, the monocultures had a lower In 2013, for both trials, plant height was related to spe- mean soil moisture than soya bean (19.8 + 3.5 and 28 + cies, density and days after planting (Table 2). Tall water- 4.1 %, respectively), but on all other consecutive DAPs, the hemp grew the tallest at the low and medium densities in opposite was apparent. Mean light intensity at the soil sur- both trials, with Palmer amaranth and uncut Japanese face for all years and trials, except Trial 2 in 2013 [see Sup- chaff flower grew to a similar height (Fig. 4AandB). porting Information—Fig. S2], had an interaction Both Palmer amaranth and uncut Japanese chaff flower between density and soya bean. Overall, light intensity at were not affected by density, whereas tall waterhemp the soil surface decreased by 25 % in 2013 and 70 % in was density sensitive. The cut Japanese chaff flower 2014 with an increase in the density [see Supporting plants were the shortest regardless of trial. In Trial 1, at Information—Fig. S2].

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Table 2. Significant effects and interactions among groups based on Amaranthaceae species competitive effect and response (field experiment) to soya bean presence/absence. Only significant differences are shown within a variable. Pooled over species. N, the number of groups in a treatment or variable; df, degrees of freedom; T1, Trial 1; T2, Trial 2; Species, study species; Soya bean, soya bean(s) present; DAP, day after planting; Density, study species density (T1: 10, 30, 90; T2: 10, 30).

Variable/effect N df FP ...... Soil moisture T1-2013: Species soya bean DAP 60 8, 110 1.76 0.0366 × × T1-2013: Density soya bean DAP 36 8, 240 4.66 ,0.0001 × × T1-2014: Soya bean DAP 12 3, 147 7.77 0.0438 × T2-2013: Species DAP 30 15, 482 2.88 ,0.0001 × T2-2013: Density soya bean DAP 48 15, 588 3.89 ,0.0001 × ×

T2-2013: Species density soya bean 40 16, 246 1.92 0.0034 Downloaded from × × T2-2014: Species DAP 30 15, 588 2.19 0.0062 × T2-2014: Soya bean DAP 12 3, 322 5.33 0.0013 × Light intensity at the soil surface

T1-2013: Density soya bean 8 2, 114 0.88 0.04184 http://aobpla.oxfordjournals.org/ × T1-2014: Density soya bean 6 2, 12.1 4.75 0.0299 × T2-2013: Density soya bean 8 3, 224 2.94 0.0338 × T2-2014: Density soya bean 6 3, 27.2 7.74 0.0007 × Species height T1-2013: Density soya bean 6 5, 90.9 4.62 0.0379 × T1-2013: Species density DAP 90 16, 158 2.23 0.0063 × ×

T1-2013: Species DAP soya bean 60 8, 110 2.94 0.0003 at Arkansas Multisite on January 21, 2016 × × T1-2014: Species DAP soya bean 60 8, 110 8.27 ,0.0001 × × T1-2014: Species density DAP 90 16, 158 3.52 0.0012 × × T2-2013: Species density DAP 120 32, 344 2.66 ,0.0001 × × T2-2014: Species DAP SB 60 21, 242 1.73 0.027 × × Soya bean height T1-2013: Species density 15 8, 24.1 3.09 0.0151 × T1-2014: Species density 15 12, 64.1 1.94 0.0345 × T2-2013: DAP density 24 12, 229 5.06 ,0.0001 × T2-2013: Species 5 4, 68 2.92 0.0305 T2-2014: DAP 6 5, 78.3 31.88 ,0.0001 T2-2014: Species density 20 12, 64.1 1.98 0.0406 × Species aboveground biomass T1-2013: Species density 15 12, 82 3.37 0.0186 × T1-2014: Species soya bean 10 4, 30 4.92 0.0067 × T2-2013: Species density soya bean 40 16, 138 2.66 0.0016 × × T2-2014: Species soya bean 10 4, 66.9 5.02 0.0013 × Soya bean aboveground biomass T1-2013: Density 3 2, 16 6.40 0.0051 T1-2014: Species 5 4, 86 15.01 ,0.0001

Continued

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Table 2. Continued

Variable/effect N df FP ...... T2-2013: Species density 20 12, 49.3 1.79 0.0757 × T2-2014: Species density 20 12, 48 2.49 0.0127 × Belowground biomass T1-2013: Species density 15 12, 102 3.53 0.0026 × T1-2014: Species density soya bean 30 8, 76.5 3.10 0.0361 × × T2-2013: Species density 15 12, 102 3.35 0.0004 × T2-2014: Species density soya bean 30 8, 76.5 3.75 0.001 × × Downloaded from Aboveground biomass was affected by study species Specifically, we considered resource drawdown as a and soya bean presence in the 2014 trials (Table 2, functional trait and competitive effect and response to Fig. 6C and D) but not the 2013 trials (Fig. 6A and B). In the soya bean crop to reflect competitive ability. A rela- both 2014 trials, the study species monocultures generally tively conservative assessment integrating all three had a greater biomass than the mixtures with soya bean. approaches would be that the competitive ability of http://aobpla.oxfordjournals.org/ Among the study species monocultures, Palmer amaranth closely related individuals with similar functional traits had the greatest biomass (3.7 + 0.7 g per pot). The cut would share invasive potential. From this perspective, Japanese chaff flower (Trial 1: 3.4 + 0.6 g) and uncut there are indications that Japanese chaff flower has Japanese chaff flower (Trial 2: 2.5 + 0.4 g) had the next high invasive potential. Thus, we advocate a multimodal largest biomass. In Trial 2, tall waterhemp showed the approach to assessing invasive potential because each opposite effect with greater biomass when soya bean approach offers a different and complimentary dimen- was present. Data on the number of branches, nodes sion of information.

and leaves are not reported since these variables showed at Arkansas Multisite on January 21, 2016 similar results to height (see Schwartz et al. 2016). Resource drawdown Neighbour species identity had a direct effect on soya The observed variation in resource drawdown among the bean biomass (Table 2). Aboveground biomass of soya four species can be explained in part by R* theory. An R* bean was affected by the interaction between study value simply is the concentration of a resource that a spe- species and density in only 2014 (2013: P NS; 2014: cies requires to survive (Krueger-Mangold et al. 2006). The ¼ P 0.01). Regardless of year and density, the highest species with the lowest R* value will outcompete a spe- ¼ soya bean biomass was in the presence of bloodleaf indi- cies with a higher R* for that particular resource (Tilman cating that it affected soya bean the least of the species 1982, 1988). Under the conditions of this experiment, (Fig. 7A and C). In 2013, the ranking of study species seedlings of Japanese chaff flower and Palmer amaranth effects on soya bean varied with density (Fig. 7A). drew down the limiting resources in a similar manner, An overall competitive effect and response ranking which indicates that at the early growth stage tested in among the study species was developed from the results this experiment, Japanese chaff flower could potentially of both the greenhouse and the field experiment based affect a crop (i.e. soya beans) in a similar way as Palmer on resource drawdown and competitive abilities. The amaranth. Thus, these species would likely displace a competitive effect ranking was determined to be: tall species such as bloodleaf that show low rates of resource waterhemp Palmer amaranth cut Japanese chaff drawdown when grown in mixture. Although bloodleaf ≥ ¼ flower uncut Japanese chaff flower . bloodleaf. The was not grown in conditions that were representative of ≥ competitive response ranking was the inverse. its native environment (i.e. sterilized soil with fertilizer and a crop versus under a forest canopy), the low drawdown of light by bloodleaf may contribute to the slow Discussion growth of this perennial species with a poor ability to col- In this study, we examined plant functional traits, com- onize. These characteristics coupled with habitat loss petitive ability and phylogenetic relatedness of four may have contributed to its endangered status in Illinois, closely related Amaranthaceae species. We assessed Maryland and Indiana (Gibson and Schwartz 2014). Fur- the invasive potential based on each of these approaches thermore, the lack of differences between the species and determined the degree of agreement between them. for N drawdown may also have been due to the short

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time frame of the experiments necessary to investigate and Oliver 1994). We hypothesize that if the experiment early seedling competition and because resin bags aver- had run longer with plants growing beyond the seedling age nutrient levels over the course of the trial (Klingaman stage, that species differences would have been seen. Downloaded from http://aobpla.oxfordjournals.org/ at Arkansas Multisite on January 21, 2016

Figure 4. The competitive response of the mean (+SE) species height for (A) Trial 2 2013, (B) Trial 1 2013, (C) Trial 2 2014 and (D) Trial 1 2014 to soya bean. Study species nomenclature is as follows: bloodleaf (IRERH), uncut Japanese chaff flower (ACHJA), cut Japanese chaff flower (ACHJA-C), Palmer amaranth (AMAPA) and tall waterhemp (AMATA). Mean values with the same letters are not significantly different at a 0.05 within a species. ¼

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Figure 4. Continued. at Arkansas Multisite on January 21, 2016

Figure 5. Competitive effect of mean (+SE) soya bean height for (A) Trial 1 2013 and (B) Trial 2 2014 in response to the species bloodleaf (IRERH), uncut Japanese chaff flower (ACHJA), cut Japanese chaff flower (ACHJA-C), Palmer amaranth (AMAPA) and tall waterhemp (AMATA). Mean values with the same letters are not significantly different at a 0.05 within a species. ¼

Ballare´ et al. (1987) proposed that the FR wavelength and initiating competitive responses through the FR/R was reflected by nearby leaves, which allowed for an phytochrome photoreceptor (Holt 1995). Novoplansky early detection of neighbouring species that signalled (1991) demonstrated Portulaca oleracea L. seedlings oncoming competition during canopy development. Thus, avoiding growth in the direction of species with higher as the seedlings in this study were growing, FR reflection reflected FR light. Thus, Japanese chaff flower with the among neighbours could have been signalling competition lowest reduction in FR light among the species tested

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Figure 6. Mean (+SE) aboveground biomass for the study species bloodleaf (IRERH), uncut Japanese chaff flower (ACHJA), cut Japanese chaff flower (ACHJA-C), Palmer amaranth (AMAPA) and tall waterhemp (AMATA) in response to soya bean for (A) Trial 2 2013, (B) Trial 1 2013, (C) Trial 2 2014 and (D) Trial 1 2014. *Above pairs of bars indicates a significant difference (a = 0.05) between mean values in aboveground biomass comparisons between monocultures and in the presence of soybean.

here may inhibit neighbouring species growing towards it. one trait (Andrew et al.2015). Japanese chaff flower Plants growing in the shade of neighbouring taller vege- attained a high competitive ranking in this study, despite tation are usually receiving reduced light intensity with not being recognized as an agricultural weed. Rankings a decreased R/FR ratio (Yang et al.2014). Thus, plants based on competitive abilities have been used in several grown under such conditions exhibit shade avoidance other studies that range from closely related weeds responses (i.e. elongated stem growth and little new (Andrew et al.2015), to less closely related weeds leaf growth) (Smith 2000). Similar responses to decreased (Horak and Loughin 2000; Bensch et al. 2003; Hock et al. light intensity during growth have been reported for Pal- 2006), or to cultivars of a single weed (Hansen et al. 2008; mer amaranth, where plasticity in acclimation to chan- Andrew et al. 2015). Although Japanese chaff flower may ging light conditions has enabled Palmer amaranth to not be fully suited to be the newest weed species in agri- develop in shade regions (i.e. under a crop canopy) and culture by escaping management strategies implemen- to achieve high rates of growth if suddenly exposed to ted by farmers (e.g. current susceptibility of Japanese high light (Patterson 1985). chaff flower to herbicide modes of action limits its spread in agricultural systems; Smith 2013; Schwartz et al. 2016), Competitive effect and response it is still an aggressive weed that farmers and land owners The competitive effect/response ranking in this study is need to be able to identify. This species has many similar novel because the species that are being compared characteristics to the Amaranthus species, such as the are within the same plant family, are found in different ability to colonize in areas with limiting resources, contin- habitats and their competitiveness varies. In addition, ual flushes of germination throughout the growing sea- competitive abilities have been based off of more than son, the ability to outcompete other weed species and

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Figure 7. Mean (+SE) aboveground biomass for the soya bean in response to the species bloodleaf (IRERH), uncut Japanese chaff flower (ACHJA), cut Japanese chaff flower (ACHJA-C), Palmer amaranth (AMAPA) and tall waterhemp (AMATA) for (A) Trial 2 2013, (B) Trial 1 2013, (C) Trial 2 2014 and (D) Trial 1 2014. Mean values with the same letters are not significantly different at a 0.05 within a species. ¼ high fecundity, but Japanese chaff flower also is a peren- waterhemp exhibit their highest germination rate of nial species that can withstand removal of shoot material 30 and 50 %, respectively, when mean air temperatures and has a high germination rate (Schwartz et al. 2016). are at 25 8C(Guo and Al-Khatib 2003). Only early detection and rapid response methods can be relied on to keep Japanese chaff flower out of areas in and around agricultural fields. If this species evolves Conclusions resistance to various herbicide modes of action, as have This research serves as an indication that the functional other taxa in the Amaranthaceae (Heap 2014), it may traits conferring competitiveness of closely related spe- well become a prominent weed in agriculture. Indeed, cies can be very similar, especially when comparing the congener Achyranthes aspera L. infests field and between invasion status (Garnier and Navas 2012). vegetable crop fields carrying with it parasitic nematodes Although the invasive species of this study, Palmer amar- (Anwar et al. 2009). anth, waterhemp and Japanese chaff flower, all exhibited Additionally, the environment plays a large role in the similar competitive and general life-history traits to one competitive effect/response of plant species. The similar- another, their habitats do not overlap much in nature. ity in competitiveness between years could be due, in Our study indicates that if these species shared the part, to the very similar environmental factors during same habitat, then the perennial Japanese chaff flower the month of May, when both trials were initiated. The could be just as competitive, if not more so, than the well- precipitation levels did vary with 9 cm of precipitation in known annual Amaranthus species. Furthermore, as a May in 2013 and 12.5 cm in 2014. Temperature is also species actively expanding its invasive range, Japanese an important ecological factor in determining species chaff flower can potentially invade other habitats, such growth and productivity. Palmer amaranth and tall as agricultural or open fields, given the right conditions.

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A Japanese chaff flower invasion into agriculture fields is Figure S1. Mean (+SE) soil moisture for (A) Trial 2 2013, currently improbable. However, pre-existing evolutionary (B) Trial 1 2013, (C) Trial 2 2014 and (D) Trial 1 2014. Red traits as seen in other Amaranthaceae species, e.g. to lines are indicative of daily average soil moisture. Mean develop herbicide resistance (Vencill et al.2008), is an values with the same letters are not significantly different evolutionary stepping stone for this species. Undoubtedly, at a 0.05 within a species. ¼ specific management tactics implemented by individual Figure S2. Mean (+SE) light intensity at the soil surface growers or managers will have a significant influence on for (A) Trial 2 2013, (B) Trial 1 2013, (C) Trial 2 2014 and (D) the rate that herbicide resistance could occur for Japanese Trial 1 2014. chaff flower, as observed in other species (e.g. Beckie et al. 2004; Evans et al. 2015). Overall, this study determined that competition Literature Cited between closely related species is driven by invasiveness Andrew IKS, Storkey J, Sparkes DL. 2015. A review of the potential for and not by life-history traits. A confamilial comparison competitive cereal cultivars as a tool in integrated weed man-

indicated that competitiveness of the perennial Japanese agement. Weed Research 55:239–248. Downloaded from chaff flower related more towards the other invasive Anwar SA, Amjad Z, Nazir J. 2009. Meloidogyne incognita infection of five weed genotypes. Pakistan Journal of Zoology 41:95–100. Amaranthus species than to the endangered native, per- Ballare´ CL, Sańchez RA, Scopel AL, Casal JJ, Ghersa GM. 1987. Early ennial bloodleaf. Resource drawdown and competition detection of neighbour plants by phytochrome perception of with soya bean was comparable between all of the inva- spectral changes in reflected sunlight. Plant, Cell and Environ- sive species, which should raise concern for other invasive ment 10:551–557. http://aobpla.oxfordjournals.org/ species in different habitats in the same geographic area. Beckie HJ, Hall LM, Meers S, Laslo JJ, Stevenson FC. 2004. Manage- More research is needed, however, to determine whether ment practices influencing herbicide resistance in wild oat. the Amaranthus species would compete in a similar man- Weed Technology 18:853–859. ner to Japanese chaff flower in a forested area and Bensch CN, Horak MJ, Peterson D. 2003. Interference of redroot pigweed whether Japanese chaff flower would compete in a (Amaranthus retroflexus), Palmer amaranth (A. Palmeri), and common waterhemp (A. rudis) in soybean.WeedScience51:37–43. soya bean field as it did in this experiment. Binkley D. 1984. Ion exchange resin bags: factors affecting estimates of nitrogen availability. Soil Science Society of America Journal 48:

Sources of Funding 1181–1184. at Arkansas Multisite on January 21, 2016 Blackburn TM, Essl F, Evans T, Hulme PE, Jeschke JM, Ku¨hn I, Partial funding was provided by the Illinois Department of Kumschick S, Markova´ Z, Mrugała A, Nentwig W, Pergl J, Natural Resources (Grant Agreement No. 13-026W) to Pysˇek P, Rabitsch W, Ricciardi A, Richardson DM, Sendek A, work on bloodleaf. Vila` M, Wilson JRU, Winter M, Genovesi P, Bacher S. 2014. A uni- fied classification of alien species based on the magnitude of Contributions by the Authors their environmental impacts. PLoS Biology 12:e1001850. Carmona CP, Rota C, Azca´rate FM, Peco B. 2015. More for less: sam- All listed authors wrote the manuscript and designed the pling strategies of plant functional traits across local environ- experiments. L.M.S. collected and analysed the data. mental gradients. Functional Ecology 29:579–588. Chesson P. 2000. Mechanisms of maintenance of species diversity. Conflict of Interest Statement Annual Review of Ecology and Systematics 31:343–366. Choi CY, Nam HY, Chae HY. 2010. Exotic seeds on the feathers of None declared. migratory birds on a stopover island in Korea. Journal of Ecology and Field Biology 33:19–22. Dıáz S, Lavorel S, De Bello F, Que´tier F, Grigulis K, Robson TM. 2007. Acknowledgements Incorporating plant functional diversity effects in ecosystem ser- The authors would like to thank Southern Illinois Univer- vice assessments. Proceedings of the National Academy of sity Carbondale, particularly the Department of Plant Sciences of the USA 104:20684–20689. Biology, and the Weed Science laboratory for support. Elton C. 1958. The ecology of invasions by animal and plants, 4th edn. London: Methuen, 181. A special thanks to Julie Young, Joseph Matthews and Evans C, Taylor DD. 2011. New invader profile: Japanese chaff flower all of the student workers (especially Travis Neal, Mike Achyranthes japonica. Wildland Weeds Summer/Fall:4–6. Murphy and Eric Janssen) for their help on various aspects Evans JA, Tranel PJ, Hager AG, Schutte B, Wu C, Chatham LA, Davis AS. of this project. 2015. Managing the evolution of herbicide resistance. Pest Management Science 72:74–80. Supporting Information Garnier E, Navas M-L. 2012. A trait-based approach to comparative functional plant ecology: concepts, methods and applications The following additional information is available in the for agroecology. A review. Agronomy for Sustainable Develop- online version of this article – ment 32:365–399.

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