Documenting the early stages of invasion of Matthiola parviflora and predicting its spread in North America.
A variety of tools have been implemented in efforts to identify potential invasions at an early stage. Deoxyribonucleic acid (DNA) fingerprinting has been suggested as a viable technique for use at ports of entry to aid in the early identification of unrecognized species of uncertain provenance (Armstrong and Ball, 2005; Van De Wiel et al., 2009). Ecologists also have worked to develop a set of traits that characterize current invasive species to predict which species may become invasive, such as high growth and reproductive rates and strong dispersal abilities (Baker, 1974; Sakai et al., 2001; Blumenthal, 2005). Modeling tools have been developed to generate habitat-suitability maps that indicate invasible regions based on the current known distribution of a focal species (Arriaga et al., 2004; Welk, 2004; Anderson et al., 2006; Ward, 2007).
Despite the suite of available tools, newly introduced species are often overlooked, even in heavily studied areas. Our study site, the Desert Laboratory at Tumamoc Hill in the Sonoran Desert in Tucson, Arizona, was established as a botanically focused ecological research station in 1903 and has been intensively studied since that time (Spalding, 1909; Bowers et al., 2006; Venable and Kimball, 2013). There are numerous plots for long-term monitoring of vegetation located throughout the reserve (Rodriguez-Buritica et al., 2013; Venable and Kimball, 2013). In 1983 and 2005, efforts were made to document the location of all nonnative species of plants (Bowers et al., 2006). The study in 2005 identified 52 nonnative species, including Matthiola longipetala (Vent.) DC [Brassicaceae] (syn. M. bicornis); however, Matthiola parviflora [Schousb.] R. Br. [Brassicaceae] was not recorded at that time.
In spring 2008, we discovered M. parviflora, previously unreported in the Western Hemisphere, growing at the Desert Laboratory. Though the precise timing of the introduction of this species to North America is uncertain, it was likely before 2005. We confirm the identity of M. parviflora with morphological and molecular analysis, provide a morphological description of M. parviflora as it appears in the Sonoran Desert, describe the distribution of M. parviflora in the Sonoran Desert over the last 3 years, and use modeling of its habitat to predict the potential future distribution of M. parviflora in North America. Our treatment of M. parviflora is one example of how to identify and determine the potential spread and density of a newly introduced species.
MATERIALS AND METHODS--We used the dichotomous key in the most recent monograph of the genus Matthiola to tentatively identify our unknown plants as M. parviflora (Conti, 1900). However, because the genus has undergone recent taxonomic revision, we consulted more recent regional floras that contained species of Matthiola in an attempt to confirm our identification (Coutinho, 1913; Zohary, 1969; Pitard and Proust, 1973; Tackholm, 1974; Maire, 1977; Ball, 1993; Livaniou-Tiniakou, 2002). These regional keys contain only subsets of the genus making definitive identification difficult. We also collected four voucher specimens and deposited them in the University of Arizona Herbarium (ARIZ; Horst 390413, 390687-390689), Tucson, as well as a voucher of M. longipetala (ARIZ; Horst 390686).
We were unable to find any previous record of M. parviflora in the New World, and some species undergo rapid evolution in a new area (Bossdorf et al., 2005; Buswell et al., 2011). Therefore, we decided to confirm our identification with DNA-sequence analysis. Total DNA was isolated from fresh leaves of M. longipetala and putative M. parviflora, both collected at the Desert Laboratory, using the DNeasy[R] Plant Mini Kit (QIAGEN, Valencia, California) according to the protocol from the manufacturer. The partial fragments of the Internal Transcribed Spacer (ITS) region (ca. 750 bp) were amplified using primers N-nc18s10 and C26A (Wen and Zimmer, 1996). Polymerase chain reaction (PCR) was performed in a 30-ml volume containing 15 ml of EconoTaq[R] PLUS GREEN 2 x Master Mix (Lucigen[R] Corporation, Middleton, Wisconsin), 1 mM of each primer, and 1 ml of template DNA. We obtained sequences of ITS from Genbank (http://www.ncbi.nlm.nih.gov/genbank/) for other species of Matthiola and several species of the closely related genus Oreoloma for use as outgroups: M. fruticulosa (DQ357566); M. capiomontiana (DQ357564); M. incana (DQ249848); M. maderensis (DQ249849); M. chorassanica (DQ518396); M. farinosa (DQ357565); M. parviflora (DQ357567 and DQ357568); Oreoloma violaceum (DQ357576); O. sulfureum (DQ357575); O. matthioloides (DQ 357574). Sequences were aligned with the computer program Sequencher 4.4 (Sequencher[R] version 4.4 sequence analysis software, Gene Codes Corporation, Ann Arbor, Michigan, http://www. genecodes.com), and phylogenies were inferred from the sequence matrix using parsimony and maximum likelihood analysis with PAUP 4.0b10 (Swofford, 2002).
Introduced populations of a species frequently exhibit morphological characteristics that differ from those in populations in their native habitat. These differences can result from plastic phenotypic responses to the new environment or rapid evolution under new selective pressures (Bossdorf et al., 2005; Buswell et al., 2011). We compared a compilation of descriptions of M. parviflora from throughout its native range with individuals in the Sonoran Desert. We examined specimens and photographs from the full range of reported populations in Arizona to ensure we thoroughly captured diversity within the population. From these records, we created a description that highlights the characteristics of the species as it occurs in the Sonoran Desert.
We discovered M. parviflora at the northern edge of the Desert Laboratory in 2008. We surveyed radially from the originally discovered plants until no more individuals were found for 20 m in all directions. Along likely dispersal channels, we extended the search 50 m beyond the last individual. We informally searched the southern sector of the Desert Laboratory, where previous surveys of exotic plants on the property had recorded the presence of M. longipetala, to see if the two species co-occurred locally (Bowers et al., 2006). No individual of either species of Matthiola was found in 2009 due to a severe winter drought. In 2010, we replicated our 2008 census. In each year, we encountered additional populations around the city of Tucson, and, in 2010, we contacted local botanical societies and distributed a flyer with photos and descriptions of M. parviflora to their members asking them to report any populations throughout the surrounding area.
Self-compatibility is a trait that is often associated with invasive plants (Baker, 1974; Sakai et al., 2001). In spring 2010, we tested the capacity for self-compatibility of M. parviflora. We located and marked 10 pairs of vegetative (pre-reproductive) plants. We randomly selected one individual from each pair to be completely enclosed in a pollinator-exclosure cage (a cone of organza cloth on a wire frame) while the other remained unmanipulated. At the end of the growing season, mature fruits were harvested, and the number of mature seeds and unfertilized ovules was counted on exclosure and control individuals.
We used MaxEnt, a species-habitat modeling software package that utilizes a maximum entropy approach (MaxEnt 3.3.2, http://www.cs.princeton.edu/~schapire/maxent/) to generate habitat-suitability maps of the native range and the predicted North American distribution of M. parviflora (Phillips et al., 2006). This software uses geo-referenced presence data and geographically explicit environmental data to create a model of requirements of habitat for a species based on its current realized niche (Phillips et al., 2006). The resulting model can then generate a map indicating predicted suitable habitat in a different geographic area (Ward, 2007).
We modeled the native Mediterranean distribution of M. parviflora using 261 records of presence from regional herbaria (Appendix). We used an additional 47 points, obtained from regional floras, for underrepresented locations in northern Africa. These additional points decreased the heavy sampling bias of the herbarium records, which favored Spain and Israel. Models from MaxEnt work most successfully when seeded with an unbiased sample of records representing the entire range of the species. However, the effect of sampling bias is negligible once the sample size reaches a threshold of ca. 100 locations of presence (Loiselle et al., 2008). Climatic data were chosen based on our assessment of those layers most biologically relevant for winter-growing plants (precipitation of coldest quarter, temperature of coldest quarter, annual precipitation, and mean diurnal range) from the Worldclim Version 1.4 dataset (www.worldclim. com) at a resolution of 2.5 arcmin (ca. 4 km). We projected the modeled niche onto a similar climatic grid of the southwestern United States and northern Mexico. We selected maximum entropy modeling because its robustness to presence-only data and low rate of omission for seeded data best fit our needs for predicting potential distribution in a new area (Phillips et al., 2006). We configured the model to use 90% of our 112 records of presence to train the model and the remaining 10% as test points for validation of the model, enough for a satisfactory test level (Pearson et al., 2007). The program MaxEnt further reduced presence bias by using only one record per cell of the climatic grid. We used the recommended defaults for the remaining parameters (Phillips et al., 2006).
RESULTS--Our unknown taxon keyed to M. longipetala or M. parviflora when using regional floras (Coutinho, 1913; Pitard and Proust, 1973; Livaniou-Tiniakou, 2002). Where a key contains both species, it keyed to M. parviflora (Conti, 1900; Zohary, 1969; Tackholm, 1974; Jafri, 1977; Maire, 1977; Ball, 1993). The fruit of most Matthiola, including M. parviflora, is a distinctive long, slender silique with short, curved horns at the tip (Fig. 1). Individuals of M. parviflora can be distinguished from M. longipetala, the only congener that occurs in North American deserts, by several vegetative and floral morphological traits (Table 1). Characters that are especially useful for differentiating the two species in the field include substantially larger corollas with wavy petals and prefloral scales in M. longipetala.
The ITs sequence for our putative M. parviflora collected in the field was 100% identical to the published ITs sequence of M. parviflora for spanish accessions in GenBank confirming our identification. Heuristic searches using maximum parsimony yielded a single phylogenetic tree, identical to the one resulting from the search using maximum likelihood. The topology of the phylogenetic tree indicated that other species of Matthiola are more closely related to M. parviflora than to M. longipetala, demonstrating that the newly discovered population is quite distinct from M. longipetala and is not a hybrid (Fig. 2).
We quote the complete species description of M. parviflora from Zohary (1969:272), which most closely represents the species as it grows in the Sonoran Desert. Additional details from other sources are added in brackets. Finally, descriptions in italics designate deviations or specifications of morphological characteristics of M. parviflora as it appears in the Sonoran Desert.
"Annual, tomentose with branched hairs, 10-30 cm 7-20 cm [Basal leaves in a rosette [+ or -] fleeting (Maire, 1977)]. Stems almost erect, diffusely branched at base. Leaves 4.5-5 (-7.5) by 0.7-1 (-1.5) cm, crowded at base and along stem, oblanceolate, sinuate-dentate or pinnatifid with acute lobes; lower leaves long-petioled, upper and floral sessile. Racemes short, often overtopped by leaves. Flowers short-pedicelled or sessile. Sepals 5 (-7) mm. Petals 0.6-0.8 (-1.5 cm) cm. [by 0.1-0.2 cm. (Ball, 1993)], purple, lavender limb with a pale yellow claw, obovate, [nectaries very small (Ball, 1993) slightly enlarged at the base (Conti, 1900)], [stamens: the large ones 3.5-4.5 mm, the small ones 2.5-3.3 mm; anthers 1.3-1.5 mm (Conti, 1900)]. Fruit 4.5-6 cm. [slightly torulose (Ball, 1993)], erect or spreading; horns 4-5 mm [straight, acute (Ball, 1993)]. [Seeds elliptic with no or little wing, 1-1.2 by 0.6-0.75 mm (Conti, 1900), numerous and pendant in a single series (Maire, 1977).] Fl. March-April."
Surveys conducted in spring 2008 around the initially discovered plants of M. parviflora on the north side of the Desert Laboratory yielded 576 individuals with most concentrated in an area ca. 150 [m.sup.2] (Fig. 3). On the south side of the Desert Laboratory, we located M. parviflora co-occurring with M. longipetala in approximately equal densities where the latter regularly occurs. We found M. parviflora, by informal searching, at five additional locations in and around Tucson. No reproductively successful adult was found in 2009.
Surveys in 2010 of the north side of the Desert Laboratory yielded 4,018 individuals concentrated in the same location as the base distribution in 2008. The identified boundary of the population had spread 70 m south and 80 m east of the boundary in 2008 following a slight downward slope for an average rate of expansion of 40 m/year. The expansion was more pronounced along slight depressions where water concentrated and then dispersed seeds in a generally linear fashion. A small number of plants dispersed a much greater distance, 225 m, via a small intermittent wash. Information from local botanical societies on location of M. parviflora yielded 38 additional populations, groups of plants separated by greater than two city blocks, throughout Tucson and two from Cave Creek, Arizona, 204 km northwest of the nearest population in Tucson.
In its native range, M. parviflora occurs in dry coastal regions and deserts. In the Canary Islands, it occupies dry coastal areas below 300 m (Pitard and Proust, 1973). It also is found in limestone hills and areas with hard sandy soil (Jafri, 1977) as well as on steppes, pastures, and floodplains in rocky dry areas from the coast to the mountains (Maire, 1977) in northern Africa. In the Middle East, M. parviflora occurs in the Negev Desert and around the Dead Sea (Zohary, 1969).
In Arizona, M. parviflora has predominantly been identified along roadsides in areas with little shade; however, observer-bias may be involved. At the Desert Laboratory, the species has spread through an area that is relatively undisturbed and has been an environmental preserve for >100 years. The majority of individuals are growing in rocky and sandy soil adjacent to dry rivulet channels or near the banks of one of the small washes that crosses the site. Individuals growing in the sandy wash itself tend to be smaller and produce fewer seeds than those growing on the banks in finer soils.
An additional factor potentially facilitating the invasion of M. parviflora is that it is self-compatible. Only three paired replicates in the self-compatibility study escaped disturbance and could be evaluated. Production of viable seeds was similar for control plants (48.5 [+ or -] 40.9%) and those in pollinator-exclosures (33.9 [+ or -] 30.7%), indicating that M. parviflora is autogamous (self-pollinates without a pollinating agent).
The native-range-niche-suitability map we produced using MaxEnt (Fig. 4a) includes all the described Mediterranean range as well as coastal Sicily, eastern Cyprus, and the eastern Grecian islands, which are areas where M. parviflora has not been recorded (Meikle, 1977; Pignatti, 1982; Strid, 1986; Livaniou-Tiniakou, 2002). Predictions from models are scored in MaxEnt by testing presence-location data against the model; random data would score 0.5. Scores evaluating our model were 0.952 for training data and 0.938 for test data. The map indicating suitability of habitat in the southern United States and Mexico identified several large regions with a high probability for being ideal habitat including a 1,200km long continuous stretch from southern Arizona, USA, to Sinaloa, Mexico, along the eastern edge of the Gulf of California (Fig. 4b). Our study site at the Desert Laboratory in Tucson, Arizona, is well within the predicted range of habitat at a level of 85-99% likelihood for suitability.
DISCUSSION--We positively identified and documented several populations of M. parviflora, a Mediterranean species not previously known to occur in the Western Hemisphere, in the Sonoran Desert, Arizona. The genus Matthiola contains ca. 140 species native to Eurasia with two species previously known to be introduced to the Western Hemisphere (United States Department of Agriculture, 2010) as escaped garden plants. Matthiola incana is found in California, Texas, Illinois, North Carolina, and British Colombia. Matthiola longipetala (syn. bicornis) is known to occur in Michigan, Kansas, Idaho, Alberta, and Saskatchewan and is widespread in the southwestern United States. It also has been documented in Tucson, Arizona since 1902 (Thornber, 1909).
It is difficult to pinpoint when the introduction of M. parviflora to the Western Hemisphere occurred. The earliest definitive record (plant is clearly identifiable) that we have found is a photograph by T. B. Kinsey taken at the eastern edge of Tucson in March 2004. The most detailed chronology of its spread comes from the Desert Laboratory, the vegetation of which has been intensively monitored since its founding by the Carnegie Institute of Washington in 1903 (Spalding, 1909; Bowers et al., 2006; Rodriguez-Buritica et al., 2013; Venable and Kimball, 2013). Efforts made in 1983 and 2005 to document the location of all nonnative species of plants by systematically walking grid lines throughout the entire reserve failed to note the presence of M. parviflora (Burgess et al., 1991; Bowers et al., 2006). However, M. longipetala (syn. M. bicornis) was recorded in the 2005 study (but not the 1983 study) at our 2008 site on the northern end of the property where M. parviflora was discovered. This was probably a misidentification of M. parviflora because we did not find M. longipetala at that location in 2008 or subsequently even though it is quite conspicuous. We have searched intensively for it, and two of those years had exceptionally high densities of winter annuals. It is difficult to say if M. parviflora was present at the time of the 1983 study but not distinguished from its congener or if it arrived later. If fruiting rather than flowering plants had been encountered during these surveys, the plants would have been readily determined as Matthiola from the distinctive fruit but perhaps not distinguished as M. parviflora, an unanticipated exotic. The most recent flora for the Desert Laboratory indicates that M. parviflora had not been recognized by 1983 even though its floral morphology is quite distinctive (Bowers and Turner, 1985). This suggests that M. parviflora arrived at the Desert Laboratory sometime between 1983 and 2005.
The early identification of invasive species is a priority for managers of land and those making public policy (Lodge and Shrader-Frechette, 2003; Blumenthal, 2005). However, early recognition of invasive species is often an elusive goal of management (Pimentel et al., 2000; Simberloff, 2003). One barrier to the goal of early recognition of introduced, potentially invasive species is the lack of a good unified key for identification. Local floras from the original native distribution, which may be fairly recently published, rarely contain all species in a genus, whereas monographic treatments, while complete, are often old (1900 in our case) and may lack important recent information on a genus. Consequently, we were not 100% confident of our initial morphological identification. However, we were able to confirm identification with sequencing and construction of phylogeny, demonstrating the power of molecular methods for quick and confident identification of possible invasive species (Armstrong and Ball, 2005; Van De Wiel et al., 2009).
Habitats likely to be invaded include heavily disturbed areas, especially locations that have experienced a recent change in disturbance regime (Moles et al., 2008). We found M. parviflora in heavily disturbed, roadside habitats and also in an undisturbed natural area. Many of the roadside populations inspected in Tucson in spring 2010 were high-density monocultures. Though it has not yet formed a dense monoculture, it also has spread rapidly through an undisturbed area of a 100-year-old nature preserve over three growing seasons.
While our surveys in the field demonstrated that M. parviflora has spread locally, results of our niche modeling indicate that this species has the potential to spread through a much larger region. Although introduced species may have slightly different niches in their new range (Broennimann et al., 2007), modeling the realized niche of a species in its home range and projecting that model to the area surrounding an introduced population allows predictions about the potential spread of a species in the new area (Welk, 2004). We identified a large area of potentially suitable habitat within North America that M. parviflora may already occupy or may expand into in the future. This indicates that M. parviflora may soon become a widespread invader over a large range (Richardson et al., 2000; Colautti and MacIsaac, 2004).
The National Park Service has been manually removing M. parviflora in Saguaro National Park East and West since 2010 and is considering chemical control. Other local managers of land also are pursuing measures of control in an attempt to prevent or slow the spread of this species in the region.
Data on the initial spread of invasive species are relatively rare but critical for understanding community-assembly, dispersal, and management of invasions (Puth and Post, 2005). The discovery of M. parviflora in North America provides an opportunity to document its early dispersal and spread and to determine its potential for invading a larger area. Our treatment of M. parviflora demonstrates how molecular techniques, surveys in the field, and niche modeling during the early stages of invasion can be used to accurately identify and determine the invasive potential of newly introduced species. Such data provide critical information for decisions on management.
APPENDIX--Herbaria providing records of specimens used for presence modeling.
Online herbaria were accessed through Global Biodiversity Information Facility Data Portal (data.gbif.org): Aranzadi Zientzi Elkartea; Botanic Garden and Botanical Museum Berlin-Dahlem; Botanical Museum, Copenhagen; CeDoc de Biodiversitat Vegetal; CIBIO, Alicante; Escuela Tecnica Superior de Ingenieros de Montes, UPM; EUNIS, European Environment Agency; Herbario de la Universidad de Granada; Herbario de la Universidad de Salamanca; Herbario de la Universidad de Sevilla; Herbarium Berolinense; Institut Botanic de Barcelona, BC-Historico; International Botanical Collections, Sweden; Israel Nature and Parks Authority; Jardin Botanico de Cordoba; Jardi Botanic de Valencia; Museum national d'histoire naturelle et Reseau des Herbiers de France; Nationaal Herbarium Nederland--Leiden Branch; Real Jardin Botanico (Madrid), Vascular Plant Herbarium; United States National Plant Germplasm System Collection; Universidad de Almeria; Universidad Complutense, Madrid; Universidad de Cordoba, Departamento de Botanica, Ecologia y Fisiologia Vegetal; Universidad de Extremadura; Universidad de Malaga; Universidad de Oviedo. Departamento de Biologia de Organismos y Sistemas; Universidad del Pais Vasco/EHU, Bilbao; Universidad Politecnica de Madrid, Banco de Germoplasma; Universidade de Santiago de Compostela; University of Reading; University of Vienna, institute for Botany. other herbaria were contacted directly: Sohag University Herbarium; Herbarium RNG at the University of Reading, United Kingdom; Hebrew University of Jerusalem Herbarium.
This research was partially supported by National Science Foundation grant DEB 0817121 (LTREB), DEB 0717380, and DEB 084478.
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Submitted 29 March 2012. Acceptance recommended by Associate Editor Florence M. Oxley 20 March 2013.
JONATHAN L. HORST, * SARAH KIMBALL, JUDITH X. BECERRA, KOJI NOGE, AND D. LAWRENCE VENABLE
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721(JLH, DLV)
Center for Environmental Biology, University of California, Irvine, CA 92697 (SK)
Department of Biosphere 2, University of Arizona, Tucson, AZ 85721 (JBX)
Department of Biological Production, Akita Prefectural University, Akita 010-0195, Japan (KN)
* Correspondent: email@example.com
TABLE 1--Morphological differences between Matthiola parviflora and M. longipetala. An asterisk denotes nonoverlapping traits which are the most useful for definitive identification in the field. Structure Substructure M. parviflora M. longipetala Overall Diffusely branched Branching from plant at base; very base; rarely leafy leafy Flower Petals * 0.6-0.8(-1.2) cm; * 1.5-2.5 by 0.2-0.7 obovate; * limb cm; * margin lavender purple or undulate; * limb brownish purple purple or pink; claw yellow, livid or purple Prefloral None * Small button-like scales * prefloral scales * Scent Not noticeably Pleasant perfume scented * in evening * Sepals 4-6 mm 8-12 mm Nectaries Very small Filiform Silique Shape Erect or spreading Upright, curved or annular Size 25-70 by 1.5-2.0 mm (30-)50-150 by 1.0-2.0(-2.5) mm Hairs Finely pubescent Densely covered with stellate with short hairs but at the branching hairs end glabrous Horns Straight acute; Strongly incurved; 1.5 mm (1.0-)2.0-10.0 mm Raceme Size <30 cm (usually 40 cm (usually <20 cm); often <50 cm); stems overtopped by rising from base leaves
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|Author:||Horst, Jonathan L.; Kimball, Sarah; Becerra, Judith X.; Noge, Koji; Venable, D. Lawrence|
|Date:||Mar 1, 2014|
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