Lonard, R.I.; Judd, F.W., and Stalter, R., 2015. Biological flora of coastal dunes and wetlands: Borrichia frutescens (L.) DC.
Borrichia frutescens (L.) DC. is a New World warm-temperate, subtropical, and tropical zone, perennial subshrub that is an important species in hypersaline coastal sites. Also known as sea ox-eye, it tolerates salinities ranging from less than 20 ppt to 130 ppt. It occurs in substrates low in organic matter and deficient in nitrogen, phosphorus, and potassium. Nearly all reproduction is vegetative from an extensive rhizome system. Populations of this species recover quickly after coverage by wrack. Stands of B. frutescens often dominate the landward border of salt marshes.
Borrichia, in the family Asteraceae, is a warm-temperate, subtropical, and tropical genus that includes two species, Borrichia frutescens (L.) DC. and Borrichia arborescens (L.) DC., one hybrid complex, Borrichia × cubana Britton and Blake, and one doubtful species Borrichia peruviana DC., known only from a vegetative type collection (Semple, 1978; Semple and Semple, 1977). Borrichia frutescens and B. arborescens are sympatric in south Florida and Bermuda, where they hybridize and produce B. × cubana (Semple and Semple, 1977).
Borrichia frutescens is morphologically variable, and it occurs throughout a broad salinity gradient, ranging from less than 20 ppt to 130 ppt (Richards et al., 2004, 2010; Semple, 1978). Borrichia frutescens is often a dominant species in high marsh sites that are only infrequently inundated. This species uses limited resources for sexual reproduction (Cattell and Karl, 2004). Vegetative reproduction by rhizomes is the primary mechanism of the lateral spread of this species into hypersaline salt pans. Herein, we review the biology of this important coastal-zone species.
TAXONOMY AND VARIATION
Borrichia frutescens (L.) DC. is a member of the family Asteraceae (Compositae) and is included in the tribe Heliantheae. The genus Borrichia was described by M. Adanson in 1763. Synonyms or rejected names for this species are Buphthalmium incanum Mill., Diomedea bidentata Cass. and Borrichia frutescens (L.) DC. var. angustifolia DC. Common names include sea ox-eye, ox-eye daisy, bush sea ox-eye, sea daisy, and bushy seaside tansy.
The following taxonomic description has been derived from Correll and Johnson, 1970; Crespo, Ruiz de León, and Rios, 2002; Everitt, Drawe, and Lonard, 2002; Gandhi and Thomas, 1989; Lehman, 2013; Lehman, O'Brien, and White, 2005; Lonard, personal observations; Radford, Ahles, and Bell, 1968; Richardson and King, 2011; and Semple, 2006.
A single, nearly translucent seed about 2.0 mm long is borne in an indehiscent achene (cypsela).
Sea ox-eye seedlings produce several pairs of glabrate, juvenile leaves with entire margins. Toothed margins are produced on more-typical blades during leaf expansion (Semple, 1978).
Borrichia frutescens is a rhizomatous, somewhat succulent, canescent or glabrate subshrub, which forms extensive colonies. Stems are erect or occasionally decumbent, are branched or unbranched, and are 0.1 to 1.5 m tall. Plant heights on Galveston Island, Texas, are usually less than 1.0 m tall. Petioles are united at their bases, up to 2 cm long, and often bearing lateral projections near the base of the blades. Leaves are simple, opposite, obovate to oblanceolate, obtuse, and apiculate. Blades are 2 to 10 cm long, 0.5 to 1.5 cm wide, and coriaceous. Epidermal surfaces are canescent. Blade margins are variable but are usually serrate-dentate or entire on the distal blades.
The inflorescence consists of globose, mostly solitary, radiate, heads (capitula) on peduncles 2 to 6 cm long. The heads are 2.5 to 3.5 cm wide and terminate the shoots. Involucres are hemispheric, about 5 mm high and 2.2 cm wide, and becoming firm with age. Phyllaries are imbricated in three to five series with the outer phyllaries somewhat herbaceous, oblong, and reflexed at maturity. The inner series is obovate, with a spine-tipped apex to 12 mm long and about 4.5 mm wide at the base. The receptacle is slightly convex and densely covered with chaff, similar to the inner phyllaries. Chaff scales are oblanceolate, 5 to 9 mm long, folded, partially enclose the achenes, and have a distal woody, orange-yellowish spine 1 to 3 mm long. Ray florets are 15 to 30, pistillate, fertile, 5 to 12 mm long, yellow or orange-tinged, and 3-toothed distally. Disc florets are bisexual, 30 to 75 per head; corolla is cylindrical, 5 to 6.5 mm long, yellow, and 5-toothed apically. The pappus is a dentate crown 0.5 to 1.0 mm long and is present on both ray and disc florets (Figure 1).
The achenes (cypselae) are dimorphic, glabrous, and black at maturity. Achenes of ray florets are three-angled and 2.5 to 3 mm long. Achenes of disc florets are four-angled, 3 to 5 mm long, and about 1 mm wide.
Borrichia frutescens is a phenotypically variable species (Richards et al., 2004, 2010; Semple, 1978). The degree of leaf serration and the size of the inflorescence vary greatly (Semple, 1978). This species occurs along a broad range of salinities, ranging from less than 20 ppt to greater than 130 ppt. Richards et al. (2004) stated that the edaphic factor of salinity defines 20 to 50% of variation in plant height in naturally occurring populations. However, Richards et al. (2010) reported that phenotypic plasticity, not adaptation to salinity levels, determines variation along a salinity gradient in coastal wetlands.
Borrichia frutescens and B. arborescens (L.) DC. are sympatric in South Florida and Bermuda where hybridization occurs (Semple and Semple, 1977). The hybrid swarm has been designated as Borrichia × cubana Britton & Blake = Borrichia cubana Britton & Blake and is intermediate in leaf pubescence and in the morphology of spines on the phyllaries (Semple and Semple, 1977). The hybrids in south Florida are maintained by assortative mating and clonal reproduction (Cattell and Karl, 2004). Hybrids typically backcross with B. frutescens, and both species and F1 hybrids occur in disturbed sites (Cattell and Karl, 2004; Semple and Semple, 1977).
In the United States, B. frutescens is distributed along the Atlantic coastline from Maryland to Florida (Adams, 1963; Antlfinger, 1981; Blake, 1951; Cattell and Karl, 2004; Guo and Pennings, 2012; Harvill, 1965; Hill, 1986; Kelley, 2006; Long and Lakela, 1971; Luken, 2012; Radford, Ahles, and Bell, 1968; Semple, 1978, 2006; Semple and Semple, 1977; Smith, 1953; Stalter and Batson, 1973; Stalter and Lamont, 1990, 1993; Stalter et al., 1999). Along the Gulf Coast of the United States, this species occurs from Florida to Texas (Alexander and Dunton, 2006; Anderson and Alexander, 1985; Correll and Johnston, 1970; Eleuterius, 1972; Heinsch et al., 2004; Judd and Lonard, 2004; Lonard and Judd, 2002; Marquardt and Pennings, 2011; Proffitt et al., 2005). In Texas, it occurs inland in the Rio Grande Delta and upstream along the Rio Grande about 200 km and has been reported in south-central Texas (Correll and Johnston, 1970; Judd and Lonard, 2002; Semple, 2006; Semple and Semple, 1977).
Borrichia frutescens occurs in coastal wetlands in Mexico, from Tamaulipas to Quintana Roo, and in inland, saline sites in San Luis Potosi and Coahuila (Correll and Johnston, 1970; Gómez-Pompa, 1973; Moreno-Casasola, 1988; Moreno-Casasola and Espejel, 1986; Sauer, 1967; Semple, 1978; Semple and Semple, 1977). Sea ox-eye has been introduced sparingly in Grand Bahamas, Cuba, and Bermuda (Semple, 1978, 2006; Semple and Semple, 1977; Thomas, 1993). Semple (1978) indicated that the occurrence of B. frutescens in Cuba and Grand Bahamas is documented by only a few voucher specimens. Recently, Crespo, Ruiz de León, and Rios (2002) reported the occurrence of sea ox-eye in a coastal site in southern Spain.
RANGE OF HABITATS
Borrichia frutescens is an important species of coastal zone vegetation in a wide variety of habitats in the United States. It is common in high salt marsh habitats that are flooded infrequently (Adams, 1963; Antlfinger, 1981, 1982; Antlfinger and Dunn, 1979, 1983; Cleary, Hosier, and Wells, 1979; Feagin and Wu, 2006; Guo and Pennings, 2012; Oosting, 1954; Stalter, 1968, 1993; Stalter and Lamont, 1990, 1993, 1997). Colonies in the high marsh are often separated by extensive areas of salt flats (Antlfinger and Dunn, 1979). In the high marsh, it also occurs in an ecotone between the low marsh, typically dominated by Spartina alterniflora, and upland sites dominated by a variety of shrubs and/or herbaceous species (Luken, 2012; Pennings and Moore, 2001; Richards, Pennings, and Donovan, 2005). Sea ox-eye occurs along estuaries and occasionally inland in south Texas and northern Mexico (Semple, 1978, 2006; Semple and Semple, 1977).
Borrichia frutescens is also an important species in the vegetation of brackish marshes (Eleuterius and McDaniel, 1978; Judd and Lonard, 2004; Lehman, O'Brien, and White, 2005; Lonard et al., 2005; Radford, Ahles, and Bell, 1968; Semple, 2006; Stutzenbaker, 1999). Bradley and Dunn (1989) found this species in disturbed sites in salt marshes in Georgia.
On Padre Island, Texas, B. frutescens occurs in nearly all topographic facets, excluding the backshore and the primary dune complex (Judd, Lonard, and Sides, 1977). It occurs in depressions in the vegetated flats and on the margins of wind–tidal flats adjacent to the Laguna Madre (Judd, Lonard, and Sides, 1977; Negrete et al., 1999; Nelson et al., 2000). In the lower Rio Grande Delta, adjacent to the Laguna Madre, B. frutescens is found in resaca (abandoned oxbows of the Rio Grande) basins, on salt flats, and in disturbed saline sites, including roadsides (Judd and Lonard, 2002; Lonard, Richardson, and Richard, 2004).
In Mexico, sea ox-eye occurs in salt marshes in the lee of primary dune complexes, in moist depressions among secondary dune complexes, and on stabilized dunes about 60 m from the high tide mark (Castillo, Popma, and Moreno-Casasola, 1991; Espejel, 1986; Gómez-Pompa, 1973; Moreno-Casasola and Espejel, 1986; Sauer, 1967).
Borrichia frutescens typically occurs in soils deficient in nitrogen, potassium, and phosphorous and in soils that are low in organic matter (Drawe et al., 1981; Profitt et al., 2005). Most of the organic matter is in the upper 15 cm of the substrate (Hanson, 1983). Hanson (1983) reported annual nitrogen fixation rates as low as 0.36 g N m−2 y−1. Substrates range from heavy clays to silty sands (Hanson, 1983; Lonard and Judd, 1981; Proffitt et al., 2005; Stiling et al., 1999; Stutzenbaker, 1999). Clay substrates in south Texas are often water-logged (Johnston, 1952, 1955).
In Tamaulipas, Mexico, Sauer (1967) noted that sea ox-eye occurred on white sand, clay and shell, quartz sand and shell, and calcareous sand. Semple (2006) indicated that B. frutescens could occur on limestone and rocky shorelines 0 to 10 m above mean high tide.
Richards et al. (2010) found that the salinity in brackish and salt marsh habitats in Georgia ranged from 4 to 127 ppt. Antlfinger and Dunn (1979) noted that salinity in other high marshes where B. frutescens is a dominant species ranged from 20 to 50 ppt. In salt flats where growth is stunted, the salinity ranges from 100 to 130 ppt (Antlfinger and Dunn, 1979). Stalter (1968) reported salinity values in the high salt marsh in South Carolina that ranged from 10 to 50 ppt. In lower areas of the high marsh, salinity ranged from 10 to 30 ppt (Stalter, 1968).
Judd, Lonard, and Sides (1977) found that 80% of the sand particle sizes ranged from 0.18 to 0.25 mm on the margins of the wind-tidal flats on South Padre Island, Texas. Depth to the water table is only 14 cm in isolated stands of B. frutescens (Judd, Lonard, and Sides, 1977).
Stalter (1968) found that the pH of salt marsh habitats in South Carolina ranged from 4.8 to 7.5 and 6.0 to 7.5 in the high marsh. Adams (1963) noted pH values ranging from 4.19 to 7.62 in high marshes in North Carolina. Drawe et al. (1981) reported pH values ranging from 7.7 to 8.4 on North Padre Island, Texas.
The natural geographical distribution of B. frutescens extends from 38°05′ N latitude on the Maryland side of Assateague Island National Seashore (Virginia and Maryland), in the temperate zone to about 20° N latitude in Quintana Roo, Mexico, in the New World tropics (Sauer, 1967; Smith, 1953; Stalter and Lamont, 1990). Borrichia frutescens overwinters in the temperate zone by producing rhizomes 15 to 20 cm below the surface (Lonard, personal observations). Borrichia frutescens maintains a typical subshrub growth form and survives during mild winters in the subtropics. Individual woody shoots may live for up to 5 years (Cattell and Karl, 2004). The northern distribution appears to be limited by the severity and duration of freezing temperatures. No freeze-tolerance studies have been reported, to our knowledge, for this species.
Plant communities on coastlines where B. frutescens occurs are typically referred to by terminology used to describe habitats and topographic zones. Communities are designated as salt marshes, brackish marshes, salt pans, salt flats, salt prairies, or estuary communities (Eleuterius, 1972; Harvill, 1965; Judd and Lonard, 2002; Kelley, 2006; Johnston 1952, 1955; Oosting, 1954; Stalter and Lamont, 1990, 1993). On South Padre Island, Texas, Judd, Lonard, and Sides (1977) associated plant communities with topographic facets. Borrichia frutescens occurs in depressions in the secondary dunes and vegetated flats, on the margins of wind–tidal flats, on the margins of hurricane washover sites, and in disturbed sites, including roadsides (Judd, Lonard, and Sides, 1977).
Johnston (1952, 1955); Castillo, Popma, and Moreno-Casasola (1991); and Moreno-Casasola and Espejel (1986) designated plant communities in coastal wetlands with species-specific nomenclature. In the Rio Grande Delta of Texas, Johnston (1952, 1955) referred to poorly drained flats that support a plant community dominated by halophytic shrubs and cacti as a Borrichia flats community. This community usually occurs on waterlogged clays 0 to 3 m above sea level. Species associated with the dominant B. frutescens include Batis maritima, Salicornia virginica, Suaeda spp., and Distichlis littoralis. In Tamaulipas, Tabasco, and Campeche, Mexico, Castillo, Popma, and Moreno-Casasola (1991) and Moreno-Casasola and Espejel (1986) identified a Borrichia frutescens–Fimbristylis spadicea = F. puberula community that occurred in wet depressions in sheltered sites on the leeward margins of foredunes. In coastal wetlands in Tabasco and Campeche, these authors identified a Borrichia frutescens community that occurred in protected and stabilized dunes about 60 m from the high tide mark, and in Campeche, they identified an Ernodea littoralis–Borrichia frutescens community in stabilized, vegetated flats. Shrubs including Coccoloba uvifera, Randia laetevirens, and Lantana involucrata characterized that assemblage. In Veracruz, Gómez-Pompa (1973) indicated that B. frutescens was an important species in “espartal” (Spartina) grasslands that are periodically inundated. Tables 1 and 2 contain representative species associated with B. frutescens throughout its range in North America and Bermuda.
Representative species associated with Borrichia frutescens in Bermuda and from Virginia to Florida.
Representative species associated with Borrichia frutescensfrom Florida to Texas and on the coastline of Veracruz, Mexico.
Borrichia frutescens is a C3 halophyte in carbon fixation with its light-independent reactions to photosynthesis (Antlfinger and Dunn, 1979). In the tropics and subtropics, photosynthesis occurs throughout the year, but winter rates of CO2 exchange are reduced (Antlfinger and Dunn, 1979). Respiration rates are similar in summer and winter (Antlfinger and Dunn, 1979).
Infrequent flooding in the high salt marsh and evaporation results in concentration of salts. Borrichia frutescens in sites of highest salinity is stunted (Antlfinger and Dunn, 1983). Salinity typically varies from 20 to 50 ppt in the high marsh and from 100 to 130 ppt in adjacent salt flats in Georgia (Antlfinger, 1981). Sea ox-eye exhibits salt-induced succulence in leaves, and the root system removes salt. The relative water content attributed to leaf succulence is 73%. Salts are sequestered within cellular vacuoles (Antlfinger, 1981).
Salinity tolerance is associated with sodium accumulation and dilution through succulence and the synthesis of nitrogen-rich compatible solutes proline and glycine–betaine (Richards et al., 2010). Ash content is high in plant tissues, which is indicative of NaCl accumulation (Lanning and Eleuterius, 1985). However, Cavalieri and Huang (1979) found that the osmoregulatory function of proline occurs only in soil salinities exceeding sea water. Cavalieri and Huang (1977) reported that B. frutescens has a salt tolerant enzyme, NAD–malate dehydrogenase, which represents a possible adaptation to a salt marsh environment.
Alexander and Dunton (2006) and Dunton, Hardegree, and Whiteledge (2001) noted that B. frutescens responds by producing greater biomass and plant cover following the reduction of salinity. Heinsch et al. (2004) found that high salinity values that occur during extended periods of tidal inundation or extended drought conditions cause this species to lose its leaves.
High sulfide concentrations in salt marshes are metabolic toxins. Both plant size and biomass are reduced by increasing concentrations of this toxin, and rhizomes are particularly sensitive (Bradley and Dunn, 1989). Clonal integration of B. frutescens stands allows rhizomatous parental clones in low-salinity sites to supply water to lateral growth, salt-stressed shoots on the high-salinity margins of the stand (Pennings and Callaway, 2000). Antlfinger (1982) found that salinity in the center of B. frutescens stands was about 15 ppt, whereas salinity was about 45 ppt on the margins of clones.
Flowering and fruiting in sea ox-eye is expected at any time of the year because of its distribution in warm–temperate, subtropical, and tropical environments (Correll and Johnston, 1970; Lonard and Judd, 1989; Rossi et al., 1999. In Maryland and Virginia, flowering occurs from July to September (Hill, 1986). Peak flowering in Mississippi is from June to August (Eleuterius and Caldwell, 1984), and in Florida, it is from May to July (Rossi et al., 1999). Gandhi and Thomas (1989) and Lehman, O'Brien, and White (2005) noted that peak flowering occurred from April to December in Louisiana and Texas. Borrichia frutescens has been introduced in coastal sites in southern Spain, where flowering has been reported from February to April, and seedlings are common after rainfall in autumn (Crespo, Ruiz de León, and Rios, 2002).
Net aerial primary productivity is often used to elucidate the growth potential of salt marsh plants. Linthurst and Reimold (1978) estimated living biomass for B. frutescens in Georgia salt marshes ranged from a minimum value of 648 g m−2 to a maximum of 1860 g m−2. They noted a fairly high litter base of dead biomass, ranging from a minimum of 184 g m−2 to as high as 291 g m−2. Stem density was high and varied from 213 m2 to 380 m2 (Linthurst and Reimold, 1978). Pennings, Stanton, and Brewer (2002) fertilized the ecotone between Spartina alterniflora and B. frutescens in salt marshes in Georgia. They found much higher productivity in S. alterniflora but a reduction in biomass and plant height of B. frutescens. They concluded that fertilization favored the low marsh-dominant species S. alterniflora (Pennings, Stanton, and Brewer, 2002).
Borrichia frutescens is a long-lived, rhizomatous subshrub that has individual stems that typically live for 5 years. Aerial shoots usually arise singly from laterally spreading rhizomes (Cattell and Karl, 2004). Elongated rhizomes enable populations to colonize barren, hypersaline salt pans (Pennings and Callaway, 2000). Rhizome lengths of plants in the saline wetlands of Galveston, Texas, are 50 cm or longer.
Population dynamics in coastal habitats is controlled by physical factors and naturally occurring and anthropocentric disturbances. Salinization influences highly clonal populations of B. frutescens to form dense stands with intense competition in crowded niches. Vegetative reproduction is enhanced.
Only a few offspring are produced by sexual reproduction (K-selection) (Blits and Gallagher, 1991; Semple and Semple, 1977). Antlfinger (1982) found that random mating and complete outcrossing occurred in B. frutescens populations. Pollen flow is only effective where 20 to 30 individuals occur within 1 m−2.
Tunnell, Withers, and Hardegree (1997) followed the recovery of B. frutescens populations in a Texas bay system following an oil spill. The site was burned to remove the oil. They found that the site, formerly dominated by B. frutescens, was dominated by Distichlis spicata several years after the fire. Lonard, Judd, and Smith (2003) noted that B. frutescens populations recovered quickly after a wild fire on the margins of the wind-tidal flats on North Padre Island, Texas. They found that B. frutescens was the only species in flower 108 days after the fire.
Borrichia frutescens is self-incompatible and depends on insects to transfer spinulose, tricolporate pollen to receptive stigmatic surfaces (Crespo, Ruiz de León, and Rios, 2002; Gandhi and Thomas, 1989). Sea ox-eye is visited by generalist pollinators, including bees, butterflies, moths, wasps, and beetles (Antlfinger, 1982; Crespo, Ruiz de León, and Rios, 2002). Bees and butterflies are the most important pollinators, and pollen exchange is weighted toward a few individuals (Antlfinger, 1982). Mean pollinator flight distance is only 40 cm between inflorescences (Antlfinger, 1982).
Borrichia frutescens is a widely distributed, New World temperate, subtropical, and tropical maritime species. Animals, including invertebrates and vertebrates, are the most likely vectors of the achenes. The firm, crown-like pappus of both ray and disc achenes may serve to aid in dispersal. Achenes may be carried on the external surfaces of birds and mammals or ingested and dispersed in feces. Tidal action may serve to move achenes over wide distances.
No data are available for seed viability after exposure to sea water.
Ungar (2001) stated that seed banks may have an important role in temporal and spatial distributions of halophytes. However, seed bank data have not been reported for this species.
Germination Ecology and Establishment of Seedlings
Crespo, Ruiz de León, and Rios (2002) noted that seedlings were abundant on sandy, saline substrates in Spain after autumn rainfall. However, Antlfinger (1981) indicated that seedling establishment was a rare event in saline wetlands in Georgia.
Salt marsh vegetation depends almost entirely on vegetative reproduction. Borrichia frutescens is a perennial clonal species that provides small amounts of resources into sexual reproduction (Cattell and Karl, 2004). Vegetative reproduction by rhizomes is the primary mechanism for the lateral spread of this species into bare patches in saline coastal wetlands and salt pans.
Stands of B. frutescens and other species in coastal wetlands are often buried by wrack deposition by abnormally high tides. Stalter et al. (2006) found that virtually all salt marsh vegetation, with the exception of Spartina patens and B. frutescens, disappeared after 2 months of coverage by wrack. Stalter et al. (2006) reported that B. frutescens was resilient even after 7 months of coverage by 15 to 25 cm of wrack.
Role in Geomorphology
Borrichia frutescens is often the climax species in saline coastal wetlands where few halophytes are adapted to that harsh environment (Tunnell, Withers, and Hardegree, 1997). The primary role in geomorphology is the stabilization of the substrate, particularly in the high marsh.
INTERACTIONS WITH OTHER SPECIES
Competition in natural plant communities is more important in communities that have favorable conditions than it is in those communities exposed to harsh physical circumstances (Bertness and Shumway, 1993). Positive or facilitation interactions among species are more often a feature of unfavorable physical parameters. Neighboring individuals or adjacent species may serve as buffers from physical stress factors (Bertness and Shumway, 1993).
In Georgia, B. frutescens dominates the landward border of most salt marshes (Pennings and Moore, 2001). The lower border of salt marshes is influenced more by physical stress than by competition, whereas the upper border of the herbaceous or grassy zone is set mostly by competition with shrubs (Pennings and Moore, 2001). Plant height and the number of leaves of sea ox-eye increase with higher elevations, and improved soil drainage promotes growth (Pennings and Moore, 2001).
Guo and Pennings (2012) found that localized oyster shell deposits altered the dynamics of salt marsh populations. The annual succulent Suaeda linearis is usually excluded by waterlogging and by perennial community dominants, including B. frutescens, Juncus roemerianus, and S. alterniflora. The physical condition of slightly elevated topography provided by oyster shell deposits produces a physical niche that provides a unique habitat for S. linearis. The niche does not allow the usual perennial dominants to colonize those sites (Guo and Pennings, 2012).
Herbivores, Predators, Parasites, and Parasitoids
Borrichia frutescens is often subjected to a wide variety of nematode infestations, insect herbivores, parasites, parasitoids, and commensalistic imperfect fungi. The nematode Tylenchulus palustris, which is closely related to roundworm infestations of commercial citrus trees, parasitizes the root system of B. frutescens (Dow et al., 1990; Tanha Maafi et al., 2012).
The gall-forming midge (Asphondylia borrichiae) may transmit the imperfect fungi Alternaria sp. and Fusarium sp. when the midge parasitizes B. frutescens (Strake, Keagy, and Stiling, 2006). Midges initiate solitary galls adjacent to the apical meristem of sea ox-eye shoots and can assume the role of a parasitoid and kill the sea ox-eye host (Stiling et al., 1992). Galls, in turn, are affected by several species of parasitoid wasps that lay eggs in the galls. Developing wasp larvae then consume the midge larvae (Strake, Keagy, and Stiling, 2006). A specialized plant hopper (Pissonotus quadripustulatus) feeds only on B. frutescens and the gall-forming midge. (Stiling et al., 1999; Stiling and Moon, 2005). Thrips (Order: Thysanoptera) have been collected from B. frutescens shoots in south Texas, but Cole and McDaniel (1964) did not indicate how those insects affect sea ox-eye populations. The angiosperm hemiparasite Cuscuta indecora (dodder) infects B. frutescens early in the growing season, but dodder usually does not kill host plants (Marquardt and Pennings, 2011).
RESPONSE TO WATER LEVELS
Borrichia frutescens is periodically inundated by high tides or less frequently by storm surges. Populations on the margins of wind–tidal flats on South Padre Island, Texas, occur where the water table is only 14 cm below the substrate surface (Judd, Lonard, and Sides, 1977). In South Carolina salt marshes, Stalter (1968) noted that sea ox-eye occurs in the high marsh and the low high marsh, in sites 1.43 to 1.81 m above mean sea level and where submergence averages 58 min d−1.
Borrichia frutescens populations may have some value in stabilization of substrates in salt marshes and brackish marshes, but its potential has not been explored. Stutzenbaker (1999) stated that sea ox-eye is not a candidate for propagation and transplantation, but the best method for propagation is to plant rhizomes in wet sites in late winter. Stutzenbaker (1999) further indicated that this perennial species does not require resource management actions.
Wildlife and Ornamental Values
Borrichia frutescens provides cover and nutrition for wildlife. Sand fiddler crabs (Uca pugilator) forage on sparsely vegetated stands of B. frutescens and S. alterniflora in South Carolina (Viscido and Wethey, 2002). In Georgia, Buck et al. (2003) found that salt marsh crabs (Armases cinereum) foraged on fresh leaves and leaf litter of sea ox-eye. In Texas wetlands, B. frutescens provides nectar for butterflies and bees and achenes for granivorous birds (Anonymous, 2013a).
On the Texas coastline, laughing gulls (Laurus atricilla), American white pelicans (Pelecanus erythrorhynchos), and roseate spoonbills (Ajaia ajaja) build nests with B. frutescens or seek cover in stands of this species (Texas Colonial Waterbird Society, 1982; Thebeau and Chapman, 1984; White, Mitchell, and Cromartie, 1982). The endangered whooping crane (Grus americana) overwinters in Texas salt marshes in plant communities dominated by B. frutescens, Batis maritima, S. alterniflora, and Salicornia spp. (Lewis, 1995). The habitat of the endangered Lower Keys marsh rabbit (Sylvilagus palustris hefneri) is coastal salt marsh prairies and buttonwood ecotones where sea ox-eye is an important species. Borrichia frutescens makes up 25% of the diet of that species (Forys, 1999).
An overlooked value for the attractive inflorescences of this species is its potential value as an ornamental. Richardson and King (2011) stated that sea ox-eye is a candidate for landscaping in saline soils that would otherwise inhibit growth of glycophytes.
We thank Glennis and David Lonard for providing assistance in the preparation of the manuscript and to an anonymous reviewer for helpful comments and suggestions. Dr. Alfred Richardson and Ken King kindly provided digital images of Borrichia frutescens.
- A.A. Abuzeineh R.D. Owen N.E. McIntyre C.W. Dick R.E. Straussand T. Holsomback 2007. Response of marsh rice rat (Oryzomys palustris) to inundation of habitat. Southwestern Naturalist, 52(1), 75–78. Google Scholar
- D.A. Adams 1963. Factors influencing vascular plant zonation in North Carolina marshes. Ecology, 44(3), 445–456. Google Scholar
- H.B. Alexander and K.H. Dunton 2006. Treated wastewater effluent as an alternative freshwater source in a hypersaline salt marsh: Impacts on salinity in organic nitrogen and emergent vegetation. Journal of Coastal Research, 22(2), 379–392. Google Scholar
- L.C. Anderson and L.L. Alexander 1985. The vegetation of Dog Island, Florida. Florida Scientist, 48(4), 232–251. Google Scholar
- A.E. Antlfinger 1981. The genetic basis of microdifferentiation in natural and experimental populations of Borrichia frutescens in relation to salinity. Evolution, 35(6), 1056–1068. Google Scholar
- A.E. Antlfinger 1982. The genetic neighborhood structure of the salt marsh composite Borrichia frutescens. Journal of Heredity, 73(2), 128–132. Google Scholar
- A.E. Antlfinger and E.L. Dunn 1979. Seasonal patterns of CO2 and water vapor exchange of three salt marsh succulents. Oecologia, 43(3), 249–260. Google Scholar
- A.E. Antlfinger and E.L. Dunn 1983. Water use and salt balance in three salt marsh succulents. American Journal of Botany, 70(4), 561–567. Google Scholar
- M.D. Bertness and S.W. Shumway 1993. Competition and facilitation in marsh plants. American Naturalist, 142(4), 718–724. Google Scholar
- L.B. Blake 1951. Erroneous record of Borrichia frutescens from District of Columbia. Rhodora, 53(632), 206–207. Google Scholar
- K.C. Blits and J.L. Gallagher 1991. Morphological and physiological responses to increased salinity in marsh and dune ecotypes of Sporobolus virginicus (L.) Kunth. Oecologia, 87(3), 330–335. Google Scholar
- P.M. Bradley and E.L. Dunn 1989. Effects of sulfide on the growth of three salt marsh halophytes of the Southeastern United States. American Journal of Botany, 76(12), 1707–1713. Google Scholar
- T.L. Buck G.A. Breed S.C. Pennings M.E. Chase M. Zimmerand T.H. Carefoot 2003. Diet choice in an omnivorous salt-marsh crab: Different food types, body size and habitat complexity. Journal of Experimental Marine Biology and Ecology, 292(2003), 103–116. Google Scholar
- S. Castillo J. Popmaand P. Moreno-Casasola 1991. Coastal sand dune vegetation of Tabasco and Campeche, Mexico. Journal of Vegetation Science, 2(1), 73–88. Google Scholar
- M.V. Cattell and S.A. Karl 2004. Genetics and morphology in Borrichia frutescens and B. arborescens (Asteraceae) hybrid zone. American Journal of Botany, 91(11), 1757–1766. Google Scholar
- A.J. Cavalieri and A.H.C. Huang 1977. Effect of NaCl on the in vitro activity of malate dehydrogenase in salt marsh halophytes of the U.S. Physiologia Plantarum, 41(1), 79–84. Google Scholar
- A.J. Cavalieri and A.H.C. Huang 1979. Evaluation of proline accumulation in the adaptation of diverse species of marsh halophytes to the saline environment. American Journal of Botany, 66(3), 307–312. Google Scholar
- W.J. Cleary P.E. Hosierand G.R. Wells 1979. Genesis and significance of marsh islands within southeastern North Carolina lagoons. Journal of Sedimentary Petrology, 49(3), 703–710. Google Scholar
- C. Cole and B. McDaniel 1964. Thrips collected from native hosts of south Texas plants. Texas Journal of Science, 16(4), 446–448. Google Scholar
- D.S. Correll and M.C. Johnston 1970. Manual of the Vascular Plants of Texas. Renner, Texas: Texas Research Foundation, p. Google Scholar
- M.B. Crespo A. Ruiz de Leónand S. Rios 2002. Borrichia Adans. (Asteraceae, Heliantheae), a new record for the Mediterranean flora. Israel Journal of Plant Sciences, 50(3), 239–242. Google Scholar
- R.L. Dow R.N. Inserra R.P. Esserand K.R. Langdon 1990. Distribution, hosts, and morphological characteristics of Tylenchulus palustris in Florida and Bermuda. Journal of Nematology, 22(4), S724–S728. Google Scholar
- D.L. Drawe K.R. Kattner W.H. McFarlandand D.D. Nehr 1981. Vegetation and soil properties of five habitat types on North Padre Island, Texas. Texas Journal of Science, 23(2–4), 145–157. Google Scholar
- K.H. Dunton B. Hardegreeand T.E. Whiteledge 2001. Response of estuarine marsh vegetation to interannual variations in precipitation. Estuaries, 24(6A), 851–861. Google Scholar
- L.N. Eleuterius 1972. The marshes of Mississippi. Castanea, 37(3), 153–168. Google Scholar
- L.N. Eleuterius and J.D. Caldwell 1984. Flowering phenology of tidal marsh plants in Mississippi. Castanea, 49(3), 172–179. Google Scholar
- L.N. Eleuterius and S. McDaniel 1978. The salt marsh flora of Mississippi. Castanea, 43(2), 86–95. Google Scholar
- T. Elsey-Quirk B.A. Middletonand C.E. Proffitt 2009. Seed dispersal and seedling emergence in a created and natural salt marsh on the Gulf of Mexico coast in southwest Louisiana, U.S.A. Restoration Ecology, 17(3), 422–432. Google Scholar
- I. Espejel 1986. La vegetacíon de las dunas de la peninsula de Yucatán, II: Sian Ka'an. Biotica, 11(1), 7–24. Google Scholar
- J.H. Everitt D.L. Draweand R.I. Lonard 2002. Trees, Shrubs & Cacti of South Texas. Lubbock, Texas; Texas Tech University Press, p. Google Scholar
- R.A. Feagin and X.B. Wu 2006. Spatial pattern and edge characteristics in restored terrace versus reference salt marshes in Galveston Bay. Wetlands, 24(4), 1004–1011. Google Scholar
- E.A. Forys 1999. Food habits of the lower Florida Keys marsh rabbit (Sylvilagus palustris hefneri). Florida Scientist, 62(2), 106–110. Google Scholar
- K.N. Gandhi and R.D. Thomas 1989. Asteraceae of Louisiana. Dallas, Texas: SMU Herbarium/BRIT. Sida, Botanical Miscellany. 4, p. Google Scholar
- A. Gómez-Pompa 1973. Ecology of the vegetation of Veracruz. In: A. Graham (ed.). Vegetation and Vegetational History of Northern Latin America. New York: Elsevier, pp. 73–148. Google Scholar
- H. Guo and S.C. Pennings 2012. Post-mortem ecosystem engineering of oysters creates habitat for a rare marsh plant. Oecologia, 170(3), 789–798. Google Scholar
- R.B. Hanson 1983. Nitrogen fixation activity (acetylene reduction) in the rhizosphere of salt marsh angiosperms, Georgia, U.S.A. Botanica Marina, 26(2), 49–59. Google Scholar
- A.M. Harvill Jr 1965. The vegetation of Parramore Island, Virginia. Castanea, 30(4), 226–228. Google Scholar
- F.A. Heinsch J.G. Heilman K.J. McInnes D.R. Cobos D.A. Zubereand D.L. Roelke 2004. Carbon dioxide exchange in a high marsh on the Texas Gulf Coast: Effects of freshwater availability. Agricultural and Forest Meteorology, 125(1), 159–172. Google Scholar
- S.R. Hill 1986. An annotated checklist of the vascular flora of Assateague Island (Maryland and Virginia). Castanea, 51(4), 265–305. Google Scholar
- M.C. Johnston 1952. Vegetation of Eastern Cameron County, Texas. Austin, Texas: University of Texas, Master's thesis, p. Google Scholar
- M.C. Johnston 1955. Vegetation of the Eolian Plain and Associated Coastal Features of Southern Texas. Austin, Texas: University of Texas, Ph.D thesis, p. Google Scholar
- F.W. Judd and R.I. Lonard 2002. Species richness and diversity of brackish and salt marshes in the Rio Grande Delta. Journal of Coastal Research, 18(4), 751–759. Google Scholar
- F.W. Judd and R.I. Lonard 2004. Community ecology of freshwater, brackish and salt marshes of the Rio Grande Delta. Texas Journal of Science, 56(2), 103–122. Google Scholar
- F.W. Judd R.I. Lonardand S.L. Sides 1977. The vegetation of South Padre Island, Texas, in relation to topography. Southwestern Naturalist, 22(1), 31–48. Google Scholar
- L. Kelley 2006. The vascular flora of Huggins Island, Onslow County, North Carolina. Castanea, 71(4), 295–311. Google Scholar
- F.C Lanningand L.N. Eleuterius 1985. Silica and ash in tissues of some plants in the coastal area of Mississippi, USA. Annals of Botany, 56(2), 157–172. Google Scholar
- R.L. Lehman 2013. Marine Plants of the Texas Coast. College Station, Texas: Texas A&M University Press, p. Google Scholar
- R.L. Lehman R. O'Brienand T. White 2005. Plants of the Texas Coastal Bend. College Station, Texas: Texas A&M University Press, p. Google Scholar
- R.A. Linthurst and R.J. Reimold 1978. An evaluation of methods for estimating the net aerial primary productivity of estuarine angiosperms. Journal of Applied Ecology, 15(3), 919–931. Google Scholar
- R.I. Lonard and F.W. Judd 1981. The Terrestrial Flora of South Padre Island, Texas. Austin, Texas: Texas Memorial Museum Miscellaneous Papers 6, p. Google Scholar
- R.I. Lonard and F.W. Judd 1989. Phenology of native angiosperms on South Padre Island, Texas. In: T. Bragg and J. Stubbendieck (eds.). Proceedings of the North American Prairie Conference. Lincoln, Nebraska: University of Nebraska, pp. 217–222. Google Scholar
- R.I. Lonard and F.W. Judd 2002. Riparian vegetation of the lower Rio Grande. Southwestern Naturalist, 47(3), 420–432. Google Scholar
- R.I. Lonard F.W. Judd J.H. Everittand M.R. Davis 2005. Remote sensing of resaca wetlands in south Texas. Proceedings of the 20th Biennial Workshop on Aerial Photography, Videography, and High Resolution Digital Imagery for Resource Assessment (Weslaco, Texas, ASPRS), pp. 232–237. Google Scholar
- R.I. Lonard F.W. Juddand E.H. Smith 2003. Recovery of vegetation following a wildfire on the margins of tidal flats, Padre Island National Seashore, Texas. Texas Journal of Science, 61(2), 83–96. Google Scholar
- R.I. Lonard A.T. Richardsonand N.L. Richard 2004. The vascular flora of the Palo Alto National Battlefield Historic Site, Cameron County, Texas. Texas Journal of Science, 56(1), 15–34. Google Scholar
- R.W. Long and O. Lakela 1971. A Flora of Tropical Florida: A Manual of the Seed Plants and Ferns of Southern Peninsular Florida. Coral Gables, Florida: University of Miami Press, p. Google Scholar
- J.D. Luken 2012. Relative stability of plant communities in a South Carolina high marsh. Castanea, 77(4), 327–334. Google Scholar
- E.S. Marquardt and S.C. Pennings 2011. Diet mixing in a parasitic plant: Adaptation or constraint? Plant Ecology, 212(1), 69–77. Google Scholar
- P. Moreno-Casasola 1988. Patterns of plant species distribution on coastal dunes along the Gulf of Mexico. Journal of Biogeography, 15(5,6), 787–806. Google Scholar
- P. Moreno-Casasola and I. Espejel 1986. Classification and ordination of coastal sand dune vegetation along the Gulf and Caribbean Sea of Mexico. Vegetatio, 66(3), 147–182. Google Scholar
- I.G Negrete A.D. Nelson J.R. Goetze L. Macke T. Wilburnand A. Day 1999. A checklist for the vascular plants of Padre Island National Seashore. Sida, 18(4), 1227–1245. Google Scholar
- A.D. Nelson J.R. Goetze I.G. Negrete V.E. French M.P. Johnsonand L.M. Macke 2000. Vegetation analysis and floristics of four communities in the Big Ball Hill region of Padre Island National Seashore. Southwestern Naturalist, 45(4), 431–442. Google Scholar
- H.J. Oosting 1954. Ecological processes and vegetation of the maritime strand in the Southeastern United States. Botanical Review, 20(4), 226–262. Google Scholar
- S.C. Pennings and R.M. Callaway 2000. The advantages of clonal integration under different ecological conditions: A community-wide test. Ecology, 81(3), 709–716. Google Scholar
- S.C. Pennings and D.J. Moore 2001. Zonation of shrubs in western Atlantic salt marshes. Oecologia, 126(4), 587–594. Google Scholar
- S.C. Pennings L.E. Stantonand J.S. Brewer 2002. Nutrient effects on the composition of salt marsh plant communities along the southern Atlantic and Gulf coasts of the United States. Estuaries, 25(6A), 1164–1173. Google Scholar
- C.E. Proffitt R.L. Chisson A.B. Owens K.R. Edwardsand S.E. Travis 2005. Spartina alterniflora genotype influences facilitation and suppression of high marsh species colonizing an early successional salt marsh. Journal of Ecology, 93(2), 404–416. Google Scholar
- A.E. Radford H.E. Ahlesand C.R. Bell 1968. Manual of the Vascular Flora of the Carolinas. Chapel Hill, North Carolina: University of North Carolina Press, p. Google Scholar
- C.L. Richards J.L. Hamrick L.A. Donovanand R. Mauricio 2004. Unexpectedly high clonal diversity of two salt marsh perennials across a severe environmental gradient. Ecology Letters, 7(12), 1155–1162. Google Scholar
- C.L. Richards S.C. Penningsand L.A. Donovan 2005. Habitat range and phenotypic variation in salt marsh plants. Plant Ecology, 176(2), 263–273. Google Scholar
- C.L. Richards S.N. White M.A. McGuire S.J. Franks L.A. Donovanand R. Mauricio 2010. Plasticity, not adaptation to salt level, explains variation along a salinity gradient in a salt marsh perennial. Estuaries and Coasts, 33(4), 840–852. Google Scholar
- A. Richardson and K. King 2011. Plants of Deep South Texas: A Field Guide to the Woody and Flowering Species. College Station, Texas: Texas A&M University Press, p. Google Scholar
- A.M Rossi P. Stiling M.V. Catelland T.I. Bowdish 1999. Evidence for host-associated races in a gall-forming midge: Tradeoffs in potential fecundity. Ecological Entomology, 24(1), 95–102. Google Scholar
- J. Sauer 1967. Geographic Reconnaissance of Seashore Vegetation Along the Mexican Gulf Coast. Baton Rouge, Louisiana: Louisiana State University Press, p. Google Scholar
- P.M. Schmidt R.A. McCleery R.R. Lopez N.J. Silvyand J.A. Schmidt 2010. Habitat succession, hardwood encroachment and raccoons as limiting factors for Lower Keys marsh rabbits. Biological Conservation, 143(11), 2703–2710. Google Scholar
- J.C. Semple 1978. A revision of the genus Borrichia Adans. (Compositae). Annals of the Missouri Botanical Garden, 65(4), 681–693. Google Scholar
- J.C. Semple 2006. Treatment of Borrichia Adanson, In: Flora of North America Editorial Committee (eds.). Flora of North America, North of Mexico, Volume 21: Magnoliophyta: Asteridae, Part 8: Asteraceae, Part 3. New York: Oxford University Press, pp. 129–131. Google Scholar
- J.C. Semple and K.S. Semple 1977. Borrichia × cubana (B. frutescens × arborescens): interspecific hybridization in the Florida Keys. Systematic Botany, 24(4), 292–301. Google Scholar
- L.B. Smith 1953. Borrichia frutescens from Chesapeake Bay. Rhodora, 55(650), 58–59. Google Scholar
- R. Stalter 1968. An Ecological Study of a South Carolina Salt Marsh. Columbia, South Carolina: University of South Carolina, Ph.D thesis, p. Google Scholar
- R. Stalter 1993. Barrier Island Botany: The Southeastern United States. Dubuque, Iowa: Brown, p. Google Scholar
- R. Stalter and W.T. Batson 1973. Seed viability in salt marsh taxa, Georgetown County, South Carolina. Castanea, 38(1), 109–110. Google Scholar
- R. Stalter A. Jung A. Starosta J. Badenand M.D. Byer 2006. Effect of wrack accumulation on salt marsh vegetation, Baruch Institute, Georgetown County, South Carolina. Transactions on Ecology and the Environment, 88, 305–313. Google Scholar
- R. Stalter and E.E. Lamont 1990. The vascular flora of Assateague Island, Virginia. Bulletin of the Torrey Botanical Club, 117(1), 48–56. Google Scholar
- R. Stalter and E.E. Lamont 1993. The vascular flora of Fort Sumter and Fort Moultrie, South Carolina, one year after Hurricane Hugo. Castanea, 58(2), 141–152. Google Scholar
- R. Stalter and E.E. Lamont 1997. Flora of North Carolina's outer banks, Ocracoke Island to Virginia. Journal of the Torrey Botanical Society, 124(1), 71–88. Google Scholar
- R. Stalter J. Tamory P. Lynchand B. Lockwood 1999. The vascular flora of Biscayne National Park, Florida. Sida, 18(4), 1207–1226. Google Scholar
- P. Stiling and D.C. Moon 2005. Quality or quantity: The direct and indirect effects of host plants on herbivores and their natural enemies. Oecologia, 142(3), 413–420. Google Scholar
- P. Stiling A.M. Rossi M. Cattelland T.I. Bowdish 1999. Weak competition between coastal insect herbivores. Florida Entomologist, 82(4), 599–608. Google Scholar
- P. Stiling A.M. Rossi D.R. Strongand D.M. Johnson 1992. Life history and parasites of Asphondylia borrichiae (Diptera: Cecidomyiidae), a gall maker on Borrichia frutescens. Florida Entomologist, 75(1), 130–137. Google Scholar
- D.T. Strake A.H. Keagyand P.D. Stiling 2006. Fungi associated with Borrichia frutescens (Asteraceae): Insect galls and endophytes. Sida, 22(1), 755–763. Google Scholar
- C.D. Stutzenbaker 1999. Aquatic and Wetland Plants of the Western Gulf Coast. Austin, Texas: University of Texas Press, p. Google Scholar
- Z. Tanha Maafi M. Amani J.D. Stanley R.N. Inserra E. van den Bergand S.A. Subbotin 2012. Description of Tylenchulus musicola sp. n. (Nematoda: Tylenchulidae) from banana in Iran with molecular phylogeny and characterization of species of Tylenchulus Cobb, 1913. Nematology, 14(3), 353–369. Google Scholar
- Texas Colonial Waterbird Society, 1982. An atlas and census of Texas waterbird colonies, 1973–1980. Kingsville, Texas: Caesar Kleberg Wildlife Research Institute, Texas A&I University, unpaged. Google Scholar
- L.C. Thebeau and B.R. Chapman 1984. Laughing gull nest placement on Little Pelican Island, Galveston Bay. Southwestern Naturalist, 29(3), 247–256. Google Scholar
- M.L.H. Thomas 1993. Mangrove swamps in Bermuda. Atoll Research Bulletin, 0(386), 1–17. Google Scholar
- J.W. Tunnell Jr K. Withersand B. Hardegree 1997. Environmental Impact and Recovery of the Exxon Pipeline Oil Spill and Burn Site, Upper Copano Bay, Texas: Final Report (1992–1995), Corpus Christi, Texas: Texas A&M University, Corpus Christi, p. Google Scholar
- I.A. Ungar 2001. Seed banks and seed population dynamics of halophytes. Wetlands Ecology and Management, 9(6), 499–510. Google Scholar
- S.V. Viscido and D.S. Wethey 2002. Quantitative analysis of fiddler crab-flock movement: Evidence for ‘selfish herd' behavior. Animal Behavior, 63(4), 735–741. Google Scholar
- D.H. White C.A. Mitchelland E. Cromartie 1982. Nesting ecology of roseate spoonbills at Nueces Bay, Texas. Auk, 99(2), 275–284. Google Scholar
- A.J. Wright R.J. Edwardsand D. van de Plassche 2011. Reassessing transfer–function performance in sea-level reconstruction based on benthic salt-marsh foraminifera from the Atlantic coast of NE North America. Marine Micropaleontology, 81(1,2), 43–62. Google Scholar