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The Endangered Pondberry (Lindera melissifolia [Walter] Blume, Lauraceae) Author(s): Margaret S. Devall Source: Natural Areas Journal, 33(4):455-465. 2013. Published By: Natural Areas Association DOI: http://dx.doi.org/10.3375/043.033.0409 URL: http://www.bioone.org/doi/full/10.3375/043.033.0409
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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. C O N S E R V A T I O N I S S U E S ABSTRACT: Pondberry (Lindera melissifolia) is an endangered plant species that occurs in seven southern states. It is a rhizomatous, clonal shrub that usually grows in colonies and has numerous stems with few branches and drooping leaves that give off a spicy odor when crushed. Pondberry is dioecious, with small yellow flowers that bloom in spring and have scarlet drupes that mature in late summer or fall. The species grows in low areas within bottomland hardwood forests in the western part of its range and on the margins of limestone sinks and wet depressions in pine forests in the eastern part. Pondberry has • probably always been a rare species, but its distribution and abundance have been affected by habitat destruction and alteration, such as timber cutting, clearing of land, and local drainage or flooding of wetlands. Until recently research on pondberry has been sparse; but because of proposed flood control measures for the area in which the species occurs in Mississippi, interest in research has increased. This review will be helpful to land managers and scientists because it provides information about all known current research on the species. The Endangered Index terms: endangered species, Lauraceae, Lindera melissifolia, pondberry
Pondberry (Lindera INTRODUCTION gitude) (Lockhart et al. 2009). Because of the proposed flood control measures, there melissifolia [Walter] Pondberry (Lindera melissifolia [Walt] was concern about the welfare of pondberry Blume, Lauraceae) was listed as an en- in the area. Studies were designed to ad- Blume, Lauraceae) dangered species in 1986 (USFWS 1986) dress these concerns, including controlled because habitat destruction and alteration, experiments in a greenhouse and in a water such as timber cutting, clearing of land, impoundment facility, and ecological stud- and local drainage or flooding of wetlands ies to understand the ecosystem dynamics had affected its distribution and abundance and sustainability of pondberry colonies (Klomps 1980; Devall et al. 2001). Pond- in the Lower Mississippi Alluvial Valley berry has probably always been a rare (LMAV). An interagency agreement was species; Steyermark discovered the plant signed in September 2002 by the U.S. Margaret S. Devall1,2 in Ripley Co., Missouri, in 1948 and stated Army Corps of Engineers, the U.S. Fish ‘So far as I know it’s one of the rarest shrubs and Wildlife Service, the U.S. Forest Ser- in the United States’ (Steyermark 1984). vice National Forest system, and the U.S. Although much of the formerly available Forest Service Research and Development, habitat has become agricultural land, pres- concerning funding and performance of 1Center for Bottomland Hardwoods ent pondberry colonies are small and oc- pondberry research (Lockhart et al. 2009). Research cupy only a part of the apparently suitable The purpose of this paper is to review all P.O. Box 227 habitat. A Recovery Plan was completed in published research articles on the species Stoneville, MS 38776 1993 (USFWS 1993), but little was known so that management recommendations about the species to inform management. resulting from the research will be avail- In the past, little published information able in one place. was available and the articles that existed contained scant quantitative data. Pondberry is a rhizomatous, clonal shrub that occurs in seasonally flooded wetlands Until recently, there has not been an in- and on the wet edges of sinks, ponds, and • tensive effort to carry out comprehensive depressions in the southeastern United research on the biology, ecology, and ef- States (Figure 1, Radford et al. 1968; De- fects of forest management on the species vall and Schiff 2002). The species usually (Devall et al. 2001; Aleric and Kirkman occurs in colonies of erect or ascending 2 Corresponding author: 2005b; Lockhart et al. 2006, 2009). Interest shoots (Figure 2). Clones usually consist [email protected] in pondberry research increased after the of numerous stems with few branches and release of the Reformulation Report for the drooping leaves that have a spicy odor when Yazoo Backwater Area in Mississippi (U.S. crushed (Devall et al. 2001; Devall and Army Corps of Engineers 2000; Lockhart Schiff 2004a). The leaves are subcordate et al. 2009). The report included plans to at the base with prominent veins on the build a large pumping station with a year- lower pubescent surface (Klomps 1980). round pump operation elevation of 26.5 m Pondberry is dioecious, with small yellow Natural Areas Journal 33:455–465 adjacent to the Steele Bayou flood control flowers that bloom in spring before leaf-out structure (32.72o N latitude, 91.01o W lon- occurs (Tucker 1984). The fruit is a scarlet
Volume 33 (4), 2013 Natural Areas Journal 455 Figure 1. Distribution map of pondberry (Lindera melissifolia, Lauraceae) in the southeastern U.S.
drupe about 1 cm long that matures in late Cartney et al. 1989). At present, there are to the Sharkey-Dowling-Alligator associa- summer or fall (Devall et al. 2001; Devall populations in Alabama, Arkansas, Geor- tions (Pettry and Switzer 1996). Dominant and Schiff 2004a) (Figure 3). The species gia, Mississippi, Missouri, North Carolina, species in the forest are sweetgum (Liquid- has a shallow root system, with rhizomes and South Carolina (USFWS 2012). The ambar styraciflua L.), sugarberry (Celtis and most roots in the upper 20 cm of soil species was collected in Louisiana be- laevigata Willd.), red maple (Acer rubrum (Wright 1989a, 1989b). fore the twentieth century (Tucker 1984; L.), Nuttall oak (Quercus nuttallii Palmer), Wurdack 1989) and recorded in Florida and box elder (A. negundo L.) (Hawkins DISTRIBUTION (Chapman 1845), but is no longer found et al. 2009a). in those states. Thomas Walter discovered pondberry in Small pondberry populations also occur in South Carolina in 1788 and described it In Mississippi, a number of pondberry Bolivar County, Sunflower County (Morris as Laurus melissaefolia (Tucker 1984). A colonies occur in the Delta National Forest, 1987), and Tallahatchee County (Heather few early naturalists (Michaux, Pursh, Nut- a bottomland hardwood forest in Sharkey Sullivan, Mississippi Natural Heritage Pro- tall, and Nees ab Eisenbeck) also collected County. The forest is crisscrossed by drain- gram botanist, pers. observation) in minor pondberry from southern states during the ages and sloughs, and seasonal flooding wooded areas surrounded by agricultural next 160 years (Steyermark 1949; Mc- occurs from late fall to spring. Soils belong land. Dominant tree species at these sites
456 Natural Areas Journal Volume 33 (4), 2013 taeda L.), pond pine (P. serotina Michx.), and swamp blackgum (Nyssa sylvatica Marshall). Pond spice (Litsea aestivalis (L.) Fernald), another rare species, also occurs here (Leonard, unpubl. data). Pondberry populations currently exist in Cumberland and Sampson Counties and it historically occurred in Bladen, Onslow, and Orange Counties (North Carolina Natural Heritage Program 2008).
In South Carolina, pondberry grows along the edges of limestone sinks and wet de- pressions, in pine forests, and more open areas (Morgan 1983). The State’s largest population occurs within an extensive de- pression area, the Honey Hill Lime-Sinks in the Francis Marion National Forest. The previously large pondberry population had decreased considerably but has been recovering after gaps were cleared around colonies (Glitzenstein 2007). Populations occur in Barnwell, Berkeley, Charleston, Figure 2. Pondberry (Lindera melissifolia, Lauraceae) colony in the Delta National Forest, MS. Dorchester, and Georgetown Counties (Jeff Glitzenstein, research associate/Beadel Fel- low at the Tall Timbers Research Station, pers. observation). include water oak (Q nigra L.), sugarberry, in northeastern Arkansas, and is the only and hickories (Carya Nutt. spp.). Poison natural occurrence in Missouri (Klomps In Georgia, as in other states in the south- ivy (Toxicodendron radicans L. Kuntze) 1980; Smith 2003). During the early 1900s, eastern coastal plain, pondberry occurs is an abundant understory species, and many bottomland hardwood forests in Mis- around the edges of limestone sinks, ponds, greenbriars (Smilax L. spp.), ladies ear- souri were cleared and other pondberry and other depressional wetlands (Wurdack drops (Brunnichia ovata [Walt.] Shinners), populations may have previously existed 1989; Aleric and Kirkman 2005b). Popula- and swamp milkweed (Asclepias perennis (Klomps 1980; Smith 2003). A planted tions occur in Baker, Calhoun, Effingham, Walter) also occur (Devall et al. 2001). population exists in Butler County (Smith Miller, Taylor, Screven, Wheeler, and 2003). Worth Counties (Georgia Department of In northeastern Arkansas, pondberry grows Natural Resources 2008; Tom Patrick, in small single-sex clones (Wright 1994). Pondberry was discovered by Samuel Georgia Dept. of Natural Resources bota- It occurs around the bottoms and edges Buckley in Wilcox County, Alabama, in nist, pers. observation), where the mostly of small seasonal ponds in bottomland 1840 and was thought to be extirpated from male plants often grow together with pond hardwood forests dominated by pin oak the state until a population of several hun- spice (Patrick et al. 1995). (Q. palustris Muenchh), willow oak (Q. dred stems was discovered in Covington phellos L.), swamp red maple (A. rubrum County in 2004 (Schotz 2005), growing Pondberry reportedly occurred in Florida, L. var. drummondi Hook & Arn. Ex Nutt.) along the western side of a shallow depres- where Chapman included the species in a Sarg.), and sweetgum (Morgan 1983). The sion forested with Nyssa biflora Walt. A list of plants growing around Quincy in ponds are located in depressions between second population was soon discovered less 1845 (McCartney et al. 1989). He sent old dunes that were formed from glacial than 1 km away (Schotz 2005). two undated specimens to the New York outwash (Saucier 1978), and which fill Botanical Garden, one labeled ‘Florida’ and with water during winter rains to a depth On the coastal plain in North Carolina, the other ‘West Florida,’ which historically of < 50 cm. The water remains until after pondberry occurs in a different habitat, at extended to the Mississippi River (Devall leafing-out occurs in spring (Wright 1990). the northeastern limit of its range, on the et al. 2001). Pondberry has not been seen Most of the surrounding land is farmed. margins of Carolina bays and wet depres- in Florida since then. Soils are loams and silty loams of the Bo- sions (Morgan 1983). These ponds have a skett-Tuckermann series (USFWS 1993). sandy substrate and tend to be fairly open Pondberry has not been found in Louisi- The pondberry population in southeastern with pondcypress (Taxodium ascendens ana in around 200 years, although it was Missouri is contiguous with the population Brongr.), red maple, loblolly pine (Pinus collected near the Ouachita River close
Volume 33 (4), 2013 Natural Areas Journal 457 to the Arkansas state line in Moorehouse and West Carroll Parishes, where it grew around ‘spicebush ponds,’ likely named for pondberry (Louisiana Department of Wildlife and Fisheries 2008). The species probably occurred at additional locations in the past, but many forested wetlands in the LMAV have been converted to other uses. Since the 1780s, 30% of wetlands in the United States have been lost (National Research Council 1992).
ASSOCIATED FORESTS
Pondberry populations occur in two general types of habitat: in low areas within bot- tomland hardwood forests in the western part of its range, and on the margins of limestone sinks and wet depressions in pine forests in the eastern part.
Hawkins et al. (2009a) collected pondberry data on five bottomland hardwood forests Figure 3. Pondberry (Lindera melissifolia, Lauraceae) fruit. in the LMAV in Mississippi, Arkansas, and Missouri. The studied portion of the St. Francis Sunken Lands had been com- mercially logged, with a diameter limit cut, in the southeastern Coastal Plain, between found that the species was photosyntheti- in the late 1970s. All the other forests had fire-maintained uplands and depressional cally competent at light levels typical of been previously cut, but the silvicultural wetlands (Aleric and Kirkman 2005b). shaded conditions, compared to competing prescriptions used were not stated. All Dominant species in the seasonally flooded understory plants such as ladies eardrops, had hydric soils and experienced seasonal depressions that Aleric and Kirkman sassafras (Sassafras albidum (Nutt) Nees), flooding in late winter and early spring, (2005b) studied were Nyssa sylvatica var. American beautyberry (Callicarpa ameri- and were without recent anthropological biflora (Walt.) Sarg. and Taxodium ascen- cana L.), and catbriar (S. glauca Walter), disturbance. Tree stem density and mean dens Brongn. One population grew under and suggested that pondberry possesses dbh were not significantly different be- laurel oak (Quercus laurifolia Michx.), the characteristics of shade plants. Wright tween plots with or without pondberry. red maple, and sweetgum. Some popula- (1990) demonstrated that pondberry grow- The sites included many flood-tolerant tions occurred across a gradient from full ing around dune ponds had high water use sun to full shade. In the Francis Marion species and similar canopy and subcanopy efficiency, which was marginally beneficial National Forest, South Carolina, pondberry species, although they differed in relative there. He concluded that pondberry pos- occupies a rather narrow zone interior importance. Canopy species at all sites sesses physiological adaptations appropri- included sweetgum, Nuttall oak, overcup to larger, less flood-tolerant shrubs, fet- ate to its habitat in Arkansas and is not at oak (Q. lyrata Walt), water oak, American terbush (Lyonia lucida Lam. K. Koch.), these sites by chance. The dune ponds are elm (Ulmus americana L.), and persimmon red bay (Persea palustris Raf. Sarg.), a benign environment where pondberry is (Diospyros virginiana L.). Two subcanopy and white bay (Magnolia virginiana buffered against several potential stresses, species occurred at all five sites: green ash L.) (Glitzenstein 2007). (F. pennsylvanica Marsh.) and American such as lack of water and competition. elm. Pondberry colonies were not associ- ated with shade tolerant or intolerant tree LIGHT ENVIRONMENT In the late 1980s, 8000 pondberry stems species or with flood tolerant or intoler- occurred in more than 50 depressions in ant species, supporting Wright’s (1990) Pondberry colonies occur in a range of the Honey Hill Lime-Sinks, in the Francis suggestion that both light from canopy habitats from deep shade to full sun. Marion National Forest, South Carolina; gaps and periodic inundation together Although Wright (1989a,b) and Klomps but in a 2001 survey, only 300 stems were promote colony establishment and suc- (1980) suggested that it requires shade, this found. In 2002, gaps were cleared around cessful growth. was untested until recently. Wright (1990) surviving pondberry colonies. Three years investigated pondberry net photosynthesis later, the total number of stems had in- Pondberry also exists in an ecotonal zone at a dune pond in northeastern Arkansas. He creased by 9% and total stem length had
458 Natural Areas Journal Volume 33 (4), 2013 increased 119% in response to the treatment female clones produced more ramets as with low ancient dunes and seasonally (Glitzenstein 2007). light availability increased. These results flooded depressions, with pondberry grow- suggest that active management to increase ing around one of the depressions. Their Aleric and Kirkman (2005b) compared light availability would be beneficial to the study demonstrated that a subsurface hy- photosynthetic and growth responses of species (Lockhart et al. 2013). drologic gradient existed between the dune rooted cuttings in a greenhouse study under slopes and pond bottom, so groundwater 100%, 42%, and 19% of full sunlight and Lockhart et al. (2007) used the product of was delivered to the pond following rain carried out a field study of four pondberry blade length and width as the independent events. A continuous clay lens under the populations in the southeastern coastal variable to develop and test a predictor of depression resulted in the water ponding plain. In the greenhouse study, growth was pondberry leaf blade area. They showed above it. 30% less in full sun than in the other two that these simple dimensions, obtained light environments. As light decreased, nondestructively, can be used to make It has long been thought that flooding is not there was decreased stomatal density, dependable predictions about how factors a physiological requirement of pondberry increased specific leaf area, and increased such as light availability, soil moisture, but that it helps to lessen competition, be- leaf area ratio. Patterns of photosynthetic and response to competition would affect cause less flood-tolerant species would be responses to different light conditions at plant growth. The model should facilitate at a disadvantage (Wright 1990; Hawkins field sites were usually similar to those future ecological and physiological stud- et al. 2009c). Also, the shaded habitat in in the greenhouse study. Photosynthetic ies, leading to better understanding of the which pondberry often occurs was thought capacity was similar to that of other shade environmental requirements for pondberry to lessen competition (Wright 1990). tolerant species. The authors suggested that growth and development (Lockhart et al. Wright (1989b) found that pondberry plants levels of sunlight < 40% are preferred, 2007). that burned during the dormant season although the species has the ability to resprouted in late May. One colony with 109 stems before the fire produced 134 adjust to a range of light environments, Lockhart et al. (2012) raised pondberry new stems, but in a colony extending up a and this should be taken into account in seedlings in a growth chamber to deter- pond bank, shrubby and herbaceous stem management of existing populations and mine effects of light availability on shoot elongation of other species was twice the reintroduction of the species. growth pattern, and leaf and stem growth. rate of pondberry, suggesting that flooding Seedlings grown in low light were 76% is helpful regarding competition. The Flooding Research Facility on the taller than those receiving high light, and Theodore Roosevelt National Wildlife had larger leaf blade dimensions, blade First-year pondberry plants in pots at varied Refuge Complex in Sharkey County, MS, area, seedling leaf area, and greater mass. densities and with different mixtures of was constructed in 1994 on land that was Seedlings exhibited a brief period of phe- male and female plants were subjected to a bottomland hardwood forest before being notypic plasticity followed by ontogenic three different treatments: (1) no flooding, cleared for agriculture. The facility was plasticity. The authors suggested that this (2) 30 day flooding, and (3) 60 day flooding recently upgraded and has 12 one-acre quality may be important in efforts to con- (Hawkins et al. 2009c). With the first two impoundments that can be independently serve and recover the species. It may allow treatments, stem height, stem diameter, and flooded or drained; the bottom of each the seedlings to respond rapidly to a brief total leaf area were significantly greater impoundment is the soil surface that was period of increased resources and maintain for male plants at lower than at higher present when agriculture ceased (Lockhart the gain through ontogenic plasticity, re- densities or for female plants regardless et al. 2006). It was used for a three-year sulting in greater competitiveness. of density. In plantings of 6, 9, and 12 study of the effects of flooding and light individuals, biomass accumulation, leaf availability on stecklings (young male Hawkins et al. (2009b) found that a hand- variables, stem height, and stem diameter and female pondberry plants produced held chlorophyll meter could be an effec- did not differ between genders. Once flood- by micropropagation), including three tive tool for estimating foliar chlorophyll ing started, both male and female plants hydrologic regimes and three light avail- concentration and content, providing a stopped stem growth and soon abscised ability treatments, with four replications. rapid, non-destructive assessment. some leaves. Single male plants were taller The stecklings were planted in 2005 and and had greater leaf biomass than females flooding treatments began in 2006 (Lock- COMPETITION, FLOODING, AND and seemed better adapted to colonize hart et al. 2006). Steckling survival, stem OTHER DISTURBANCE suitable habitat, which may contribute to length, and stem diameter growth were the male-biased colonies seen in nature. only slightly affected by hydroperiod, but Pondberry is exposed to inundation from However, the authors found no evidence soil flooding may be important for reduc- flooding, but little is known about the that competitive exclusion occurred during tion of interspecific competition. Survival hydrological characteristics of its habitat. the pre-reproductive growth stage. In high and stem length growth were best with Priest and Wright (1991) used piezometers density plantings (≥ 6 plants), no difference 37% light, and stem diameter growth to study the groundwater hydrology of a was recorded in size or growth variables was greatest with 70% light. In addition, pondberry colony in Arkansas, in an area in male and female plants.
Volume 33 (4), 2013 Natural Areas Journal 459 The most numerous pondberry popula- fruited heavily seemed prone to dieback. He a wetland margin. Each treatment was tions occur in bottomland forests of the found no effective seed bank, even where randomly assigned to a 1.0-m2 subplot with LMAV, which generally flood from late fruit production had been heavy. Wright five seeds per treatment and no replication winter to early spring, with no apparent (1994) recorded a male/female ratio of due to flooding of some plots. Neither lit- ill effects to mature plants (Wright 1990; 7:1, and found that male stems had 20% ter presence nor sowing depth influenced Hawkins et al. 2009c). The species may be higher stomatal conductance. Richardson et seed germination, but more caged seeds ecologically adapted to flooding when the al. (1990) reported that female pondberry germinated when pulp was removed. In a plants are dormant. Hawkins et al. (2009c) stems in Jackson Co., Arkansas, produced shade-house study, there was no difference demonstrated that first-year, metabolically significantly fewer flowers (29.5 ± 4.3 ♀, in germination of seeds in a flooded treat- active plants are not adapted to endure ex- 62 ± 7.9 ♂) and leaves per branch than ment planted 2.5 cm deep and non-flooded tended (≥ 30 days) flooding. Little height males (6.1 ± 0.1 ♀, 6.6 ± 0.1 ♂), but ex- treatments at 2.5 cm and 5.0 cm. growth occurred after flooding began, leaf hibited no other difference in morphology. turgor declined, and some leaf abscission The sex ratio was male-biased, and female Connor et al. (2006, 2007) investigated occurred after 10 – 14 days. Wright (1990) clones covered less area and had lower the early physical and biochemical char- suggested that since flooding of 7 – 10 stem density. They marked and reexam- acteristics of maturing pondberry fruit. days during the growing season promotes ined female stems and found no evidence Over half of the fruit were aborted dur- ramet production; short-term flooding may of sex change. Two spicebush (Lindera ing the first three months, and then loss promote colony expansion. benzoin) plants that produced only male decreased. Three months after flowering, flowers in 1980 and 1982 produced both drupes reached mature size; and seeds Hawkins et al. (2010) also studied the hy- male and female plants in 1983 and 1984 reached mature size a month later. Aver- drologic regime and floristic composition (Primack 1985). age seed diameter was 6.6 mm and weight of pondberry colonies in three populations was 0.18 g. The dominant fatty acid in the in Mississippi. They identified 69 plant Devall et al. (2001) investigated pondberry seeds was lauric acid. Oleic and linolenic species that occurred within colonies. reproductive biology in Mississippi and acids were present in fairly large quantities Although floods and their duration varied Arkansas. At the Delta National Forest, and there were traces of palmitic, stearic, among the three populations, plant com- male stems produced a mean of 10.9 and linolenic fatty acids. Seeds without pulp, buried for two months, and kept in position of the colonies and the ratio of flower clusters and female stems produced 6.4 flower clusters with 4.0 flowers per an incubator for eight weeks, had 53% pondberry to other plants remained fairly cluster in early March. In early October, germination. Seeds do not germinate im- stable during the three-year study. They there were 0.8 mature fruits per female mediately after dispersal (Connor 2007). concluded that vines capable of growing stem (3.2% fruit set). Six flower clusters Fully hydrated seeds could be stored suc- over the pondberry plants (Smilax spp. and covered with mesh bags produced no cessfully for 16 months at both 4 oC and Vitis spp.) have the greatest potential to fruit, indicating that pollen is not moved 2 oC. Dried seed showed low levels of become strong competitors in this area. by wind. Flowers supplemented with germination compared to fully hydrated pollination via an artist’s brush did not seeds when conventionally stored at 4 These studies suggest that, like baldcypress produce significantly more fruit than open oC, but they could be successfully stored (Taxodium distichum (L.) Rich), seedlings pollinated flowers. At Corning, Arkansas, in liquid nitrogen, which is encouraging that can only tolerate submergence for a male stems produced 15.0 clusters and for long-term germplasm conservation. short period (Demaree 1932), pondberry 6.8 flowers per cluster. Females produced The authors suggested that pondberry seedlings should survive and grow better 12.3 clusters and 5.8 flowers per cluster. seeds are ‘sub-orthodox,’ intermediate in the field in a year with less than average Female stems produced 11.5 mature fruit between ‘orthodox’ seeds, which can be flooding, but a colony benefits from annual per stem (16.2% fruit set). dried to moisture content of < 12% and flooding to reduce competition. ‘recalcitrant’ seeds, which must be stored fully hydrated. Although pondberry may FRUIT AND SEED CHARACTERISTICS increase more by vegetative reproduction, REPRODUCTIVE BIOLOGY Connor et al. (2007) concluded that fruit Information on the best methods of plant- and seed production may be important in Information about reproductive biology ing pondberry seeds has been lacking, and the survival of the species. With sufficient would help to recover an endangered spe- nothing was known about seed storage. light and moisture and no late frosts, a cies, but very little was known about pond- Aleric and Kirkman (2005a) tested germi- stem can produce several hundred fruits. berry reproductive biology until Wright nation of seeds placed on the soil surface Morgan (1983) and others (M. Devall, pers. began to carry out research. Wright (1989a) with litter and no litter, pulp and no pulp, observation) never observed seedlings in found that fruit set (when one can see which and cage and no cage, using a three-factor the field although seed production was flowers have at least temporarily produced design, including two additional treatments successful. a fruit) in several populations of pondberry (with litter, no pulp, and no cage) of dif- was erratic, abundant in one year, and ferent planting depths (2.5 cm and 5.0 Connor et al. (2012) examined the survival scarce the next two years, and stems that cm). A 10-m2 plot was established along of seeds in mesh bags kept in a soil seed
460 Natural Areas Journal Volume 33 (4), 2013 bank for up to a year. They found that the cardinalis L.) were observed eating the dieback and resprouting. By the third year, presence or absence of fruit pulp did not fruits. Northern cardinals, pondberry seed 44.2% of planted seeds had germinated and significantly affect seed survival, but buried predators, were observed crushing seeds 53.6% by the seventh year, but survival was seeds were seven times more likely to pro- before eating them. Hermit thrushes ate very low. By 2000, three of five cohorts duce seedlings in the field than seeds left whole seeds and soon regurgitated them, (seedlings that germinated in a calendar on the soil surface. They suggested that it but other birds and mammals, such as the year) had not survived and survival of the is environmental conditions or other biotic raccoon (Procyon lotor (L.)), black bear other two cohorts was < 10%. factors that limit the presence of pondberry (Ursus americanus Pallas), and Virginia seedlings in the field. opossum (Didelphis marsupialis (L.)) may PROPAGATION be pondberry dispersers as well (Smith et Hawkins et al. (2011) investigated pond- al. 2004). Large numbers of plants of similar physi- berry seed ecology to determine if it con- ological age and size are needed for some tributes to the species’ rarity. They found Abilio et al. (2008) used a recording video studies, but are often unavailable, especially that the absence of a persistent soil bank, no camera with infrared illumination to moni- with an endangered species. Hawkins et al. obvious long-distance dispersal, and late- tor animal visitors to seed plots in or near (2007) describe a pondberry micropropa- season germination that affects survival the Delta National Forest. At each location, gation protocol developed by Deborah during floods and in the following winter a one-meter2 plot was established and 25 McCown at Knight Hollow Nursery using may contribute to the continued rarity. pondberry seeds were arranged on the soil shoot cultures under the auspices of the surface inside the plot. The animals identi- U.S. Forest Service Center for Bottomland Oh et al. (2012) found that essential oil fied as possible pondberry seed predators Hardwoods Research, Stoneville, MS. The from pondberry drupes has a significant tick were the northern cardinal, brown thrasher protocol was successful and more than repellent effect and a moderate mosquito- (Toxostoma rufum Linn.), swamp rabbit 10,000 stecklings representing 20 male repellent effect. Plant-based repellents may (Sylvilagus sp.), nine-banded armadillo and female genotypes were produced and have less harmful side effects than other (Dasypus novemcintus L.), and gray squir- used in field and controlled studies. This repellents (Oh et al. 2012). rel (Sciurus carolinensis Gmelin). protocol was necessary in order to avoid DISPERSAL EXPERIMENTAL PLANTING depleting natural populations and to pro- vide plants representing a cross-section of After Steyermark found pondberry in Tucker (1984) reported that no controlled genotypes from the area, allowing for more southeastern Missouri, 643.6 km from the propagation techniques for pondberry were uniform experimental materials. nearest pondberry population, Cora Stey- known. In order to advance protection ermark asked: “How do you account for of the species, several scientists have at- Devall et al. (2004b) translocated young this berry bouncing 400 miles? It wasn’t tempted to propagate the species. Wright male and female pondberry stems from a dropped here from a plane” (Steyermark (1989a) sowed pondberry seeds in the natural population as an aid in conserving 1984). Ridley (1930) stated that many plant greenhouse in the fall and transplanted 64 the species. They planted the stems in species that grow near lakes and ponds, seedlings to an existing colony around a pots and introduced them to five protected but not in running water, are widely scat- pond in Arkansas between April and June. locations in the field, on National Wildlife tered, often over a large area, similar to Survival after 4 – 5 months ranged from Refuges, and in a State Park. After a year, pondberry distribution. Passive dispersal 10% – 89%. The author did not publish 69% of the plants survived, with male and of pondberry seeds by water may have subsequent survival data. female plants having equal survival rates. occurred in the past (Smith et al. 2004), More than 90% of the surviving plants but flood control projects have thoroughly The Missouri Department of Conservation had increased height, although the height altered Mississippi Alluvial Valley hy- planted first-year pondberry seedlings in of the tallest stems decreased. Many of the drological cycles (Sharitz 1992; Stanturf a protected forest in Butler Co., near the plants produced new stems, but some older et al. 2000), so water probably has little naturally occurring population in 1990, stems died during the year. However the opportunity to disperse pondberry in that and sowed seeds from the Sand Ponds long-term survival after three years was area today. Smith et al. (2004) suggested plants at both sites in 1993 (Smith 2003). poor, and by 2011 only two plants survived that the combination of showy fruits and Seed handling included removal of the (M. Devall, pers. observation). persistence on the stem suggested that fruit pericarps and seed stratification. For animals, especially birds, may be dispersers field-sown seeds, pericarps of the fruits GENETIC DIVERSITY of the fruit. Smith et al. (2004) observed were removed, the seeds were washed fruiting colonies of pondberry and recorded in water, and then planted 1 – 3 cm deep Knowledge of the genetic structure of a spe- 82 bird species in the vicinity of colonies within one day of collection. Eleven (7.1%) cies can aid conservation and management and 12 species on pondberry plants. The planted seedlings survived from 1990 to strategies. Rare and endangered species hermit thrush (Catharus guttatus Pallas) 2000 and their average height was slightly often have low levels of genetic diversity and the northern cardinal (Cardinalis shorter than their height at planting due to due to historical or ecological causes (Godt
Volume 33 (4), 2013 Natural Areas Journal 461 and Hamrick 1996). Allozyme diversity of ing and found heterozygote excess in four Leafcutter bees (Megachilidae) cut circu- 15 pondberry populations from Missouri of the eastern populations. This occurs in lar sections from the edges of pondberry to the Carolinas was evaluated by Godt clonal populations, and is a result of self- leaves, and Smith (2003) noted that in and Hamrick (1996). The species exhib- incompatibility in dioecious species and in some years they remove the majority of ited low levels of allozyme diversity and obligate outcrossing hermaphrodites (Bal- leaf tissue from a stem. These bees are little genetic variation at 27 loci. Nine of loux 2004). It can also occur in populations also present in the Delta National Forest, the 27 loci were polymorphic, but genetic that have experienced a recent population Mississippi, but they have not caused ex- diversity at these loci was low and not bottleneck, a severe reduction in size tensive damage at that location (M. Devall, many were polymorphic within popula- (Cornuet and Luikart 1996). The authors pers. observation). tions. The results indicated that pondberry suggested that a conservative plan for in- Xy- is genetically depauperate compared to creasing biological diversity in pondberry The Asian redbay ambrosia beetle ( leborus glabratus Eichoff) was first de- spicebush and other woody species, which populations would be to limit germplasm tected near Savannah, Georgia in 2002, often maintain high levels of genetic diver- transfers to within a region. They recom- and mortality of redbay (Persea borbonea sity. The family Lauraceae is not geneti- mended that pondberry seed nurseries be (L.) Spreng) occurred nearby soon after. cally depauperate, and diversity occurs in established to allow crossing among a wide The beetle carries the laurel wilt pathogen avocado (Persea americana) Torres et al variety of regional genotypes, which could (Raffaelea lauricola (TC Harr., Fraedrich (1978). Many of the populations consisted provide the diverse seed sources necessary & Aghayeva sp. nov.), which causes a of only one or a few genets (genetically for restoration programs. They cautioned vascular wilt disease in members of Laura- identical individuals) with mostly or all that propagating vegetative cuttings from ceae. Fraedrich et al. (2011) demonstrated male clones. The authors suggested that existing colonies would not increase total that pondberry and pondspice were highly the low genetic diversity of pondberry may genet diversity. susceptible and isolated the pathogen from be caused mainly by bottlenecks during some diseased pondberry plants in the field. its evolutionary history and recommended The authors suggested that pondberry and DISEASES AND HERBIVORES that genetic diversity within populations pondspice may not be attacked frequently be increased by increasing population Dead stems and live stems with dead tops by the beetles because they are shrubs with sizes and enhancing sexual reproduction may be observed scattered through many small diameter stems. to lessen the risk of extinction, but did not pondberry populations. It was thought specify how this should be done. CONCLUSION that a fungus might be responsible, but Echt et al. (2006) developed microsatellite no information was available on the actual A lot has been learned about pondberry markers for genetic studies of pondberry. cause. Devall et al. (2001) recorded dead as a result of the recent studies. Although Information on gene flow, inbreeding, stems (7.1% to 57.9%) or stems with die- the species can adjust to a range of light and genetic structure within and among back (7.4% to 33.8%), in 20 visits to four environments, Aleric and Kirkman (2005b) colonies is scarce or nonexistent, and it pondberry populations in Mississippi and and Lockhart et al. (2013) suggested that is not known whether genetic diversity is Arkansas. They isolated eight fungal spe- levels of sunlight around 40% seem to be declining. This information would be help- cies from pondberry stems, three of which best in management and reintroduction ful for determining if the self-sustaining had been previously reported from Lindera: of the species. Wright’s studies indicated populations that are required for delisting Cercospora, Diaporthe and Colletotrichum that some flooding is helpful in reducing under the USFWS Recovery Plan (1993) (= Gloesporium). Morgan (1983) noted that competition, and he suggested it may even exist and in establishing best conservation 56% of flowering stems in a population promote colony expansion through ramet practices (Echt et al. 2006). in Missouri died back during the growing production. While flooding in late winter season, partially due to an abnormally and spring has no apparent ill effects on dry summer. Twenty years later, 14.5% Echt et al. (2011) quantified popula- mature plants, Hawkins et al. (2009c) tion genetic differentiation and diversity to 31.3% of dead stems occurred in the found that introduced young plants should among 450 genets in 10 locations across contiguous Arkansas population, and it the range of pondberry (all states except was growing vigorously (Devall et al. be protected from extended flooding. Re- Missouri) using 11 microsatellite loci. 2001), suggesting that the die-back does garding competition, vines that grow over They determined that the largest pairwise not completely kill a colony. pondberry plants are the worst competitors regional difference occurred between (Hawkins et al. 2010). Connor et al. (2007) eastern and western population groups, Several insects are known to feed on found that seeds do not germinate imme- and the northern population groups in each pondberry, but most do not cause severe diately after dispersal, and fully hydrated region diverged more from each other than damage. The common swallowtail (Papilio seeds can be stored successfully for 16 the southern groups. Genetic diversity was troilus) uses pondberry as a larval food months at both 4 oC and 2 oC. Connor et the lowest in the Sand Pond Natural Area in the Sunflower County, MS, population al. (2012) found that buried seeds were and highest in the Francis Marion National (Morris 1989), but only damages a few significantly more likely to produce seed- Forest. They found no evidence for inbreed- leaves (M. Devall, pers. observation). lings than seeds on the soil surface, and
462 Natural Areas Journal Volume 33 (4), 2013 suggested that environmental conditions or This review of all published research acid composition, and storage of drupes and other biotic factors limit the presence of articles on pondberry, and the recom- seeds from the endangered pondberry (Lin- pondberry seedlings in the field. mendations provided, should be helpful to dera melissifolia). Biological Conservation land managers and scientists working on 137:489-496. Echt et al. (2011) suggested limiting pondberry maintenance and recovery. Connor, K.F., G.M. Schaefer, J.B. Donahoo, M.S. Devall, T.S. Hawkins, E.S. Gardiner,T. germplasm transfers within a region. D. Leininger, A.D. Wilson, N.M. Schiff, They recommended establishment of seed and PB. Hamel. 2012. A one year Lindera nurseries rather than propagation of vegeta- ACKNOWLEDGMENTS melissifolia (Walt.) Blume seed bank study tive cuttings to increase genetic diversity. in a bottomland hardwood forest. Seed Although some information is available, We thank the U.S. Army Corps of Engi- Technology 34:163-172. more research on fruit dispersal, seed neers, the U.S. Fish and Wildlife Service, Connor, K.F., G.M. Schaefer, J. Donahoo, M. banks, and seed germination is needed. and the U.S Forest Service Southern Re- Devall, E. Gardiner, T. Leininger, D. Wilson, Active vegetation removal or other man- search Station for underwriting the cost N. Schiff, P. Hamel, and C. Echt. 2006. A study of the early fruit characteristics of agement prescriptions may be essential of this research. We are grateful to Craig pondberry. Pp. 564-568 in K.F. Connor, ed., for maintaining the existence of some Echt for helpful discussions concerning Proceedings of the 13th Biennial Southern colonies. Some monitoring of pondberry self-sustaining populations. We thank Silvicultural Research Conference. General populations is being carried out by Natural Steven Hughes for preparing the distribu- Technical Report SRS-92. U.S. Department Heritage Commissions and by interested tion map. of Agriculture, Forest Service, Southern scientists, but a better coordinated effort to Research Station, Asheville, N.C. monitor the species would be helpful. The Cornuet, J.M., and G. Luikart. 1996. Description U.S. Fish and Wildlife Service serves as a and power analysis of two tests for detecting clearinghouse of information on pondberry Margaret Devall is a plant ecologist with recent population bottlenecks from allele and conducts 5-year reviews based on the the U.S. Forest Service, Center for Bot- frequency data. Genetics 144:2001-2014. best available information. tomland Hardwoods Research in Stonev- Demaree, D. 1932. Submerging experiments ille, MS. Her research interests include with Taxodum. Ecology 13:258-262. Pondberry is a difficult species to evalu- ecology and conservation of pondberry, Devall, M., and N. Schiff. 2002. A guide to ate for change in its status as endangered. ecology of forested wetlands, and den- finding pondberry (Lindera melissifolia). Numerous ramets may be present in a drochronology. Science Update SRS-3, U.S. Department colony, but this can be deceptive because of Agriculture, Forest Service, Southern Research Station, Asheville, N.C. they all may be male or all female, or they LITERATURE CITED Devall, M.S., and N. M. Schiff. 2004a. (Lindera may be part of a single genet or a very Abilio, F.M., C. Smith III, C. Tidwe1l, P. Hamel, melissifolia [Walt] Blume) Lauraceae. Pp. few. The Recovery Plan for pondberry M. Deva1l, and T. Leininger. 2008. Pond- 440-441 in John K. Francis, ed., Wildland (USFWS 1993) states that its status will berry (Lindera melissifolia) seed predators. Shrubs of the United States and its Ter- be changed from endangered to threatened E-Proceedings C54-2, IV Congreso Forestal ritories: Thamnic Descriptions: Vol. 1. “when there are 15 protected, self-sustain- Latinoamericano, Merida, Venezuela. General Technical Report IITF-GTR-26, San Juan, P.R., USDA Forest Service, Aleric, K.M., and L.K. Kirkman. 2005a. Seed ing populations distributed throughout the International Institute of Tropical Forestry germination observations of the feder- species’ historic range.” New populations and U.S. Department of Agriculture, Forest ally listed Lindera melissifolia. Castanea have been discovered, but it is unclear if Service, Rocky Mountain Research Station, 70:157-160. recovery is progressing. The Plan does not Ft. Collins, Colo. Aleric, K.M., and L.K. Kirkman. 2005b. Growth Devall, M., N. Schiff, and D. Boyette. 2001. define a self-sustaining population or the and photosynthetic responses of the feder- Ecology and reproductive biology of the specific geographic distribution required, ally endangered shrub, Lindera melissifolia endangered pondberry (Lindera melissifo- but this information should be part of the (Lauraceae), to varied light environments. lia [Walt] Blume). Natural Areas Journal plan. We suggest a definition of a self- American Journal of Botany 92:682-689. 21:250-258. sustaining population: as an area of at Balloux, F. 2004. Heterozygote excess in Devall, M.S., N.M. Schiff, and S.A. Skojac. 2 least 1 km containing at least 50 distinct small populations and the heterozygote- 2004b. Outplanting of the endangered pond- and unrelated pondberry genets distributed excess effective population size. Evolution berry. Pp. 574-577 in Kristina F. Connor, ed., across its extent, having a female:male 58:1891-1900. Proceedings of the 12th Biennial Southern sex ratio between 0.75 and 1.25 (ideally Chapman, A.W. 1845. A list of the plants grow- Silvicultural Research Conference. General ing spontaneously in the vicinity of Quincy, Technical Report SRS-71, U.S. Department 1.0), and with each genet at reproductive Florida. The Western Journal of Medicine of Agriculture, Forest Service, Southern maturity growing either singly or clon- and Surgery 3:461-483. Research Station, Asheville, N.C. ally. Under this definition, populations are Connor, K.F., G.M. Schaefer, J. Donahoo, Echt, C.S., D. Deemer, D. Gustafson. 2011. distinct when situated farther than 2 km M. Devall, E. Gardiner, T. Leininger, T. Patterns of differentiation among endangered from the edge of next nearest pondberry Hawkins, D.Wilson, N. Schiff, P. Hamel, pondberry populations. Conservation Genet- population. and T. Leininger. 2007. Development, fatty ics 12:1015-1026.
Volume 33 (4), 2013 Natural Areas Journal 463 Echt, C.S., D. Deemer, T. Kubisiak, and C.D. Klomps, V.L. 1980. The status of Lindera sion on Geosciences, Environment and Nelson. 2006. Microsatellites for Lindera melissifolium (Walt.) Blume, pondberry, in Resources. 1992. Restoration of Aquatic species. Molecular Ecology Notes 6:1171- Missouri. Transactions Missouri Academy Ecosystems, Science, Technology, and 1173. of Science 14:61-66. Public Policy. National Academy Press, Washington, D.C. Fraedrich, S.W., T.C. Harrington, C.A. Bates, J. Lockhart, B.R., E.S. Gardiner, T.D. Leininger, Johnson, L.S. Reid, G.S. Best, T.D. Leini- K.F. Connor, P.B. Hamel, N.M. Schiff, A.D. North Carolina Natural Heritage Program. 2008. nger, and T.S. Hawkins. 2011. Susceptibility Wilson, and M.S. Devall. 2006. Flooding Lindera melissifolia – pondberry. Available to laurel wilt and disease incidence in two facility helps scientists examine the eco- online
464 Natural Areas Journal Volume 33 (4), 2013 first observed dispersal agent for pondberry Main report, Supplement No.1, and Appen- Wright, R.D. 1989b. Species biology of Lindera (Lindera melissifolia). Castanea 69:1-8. dices 1-4, vol. 1. U.S. Department of De- melissifolia (Walt.) Blume in northeast Ar- Stanturf, J.A., E.S. Gardiner, P.B. Hamel, M.S. fense, Army Corp of Engineers, Vicksburg kansas. Pp. 176-179 in R.S. Mitchell, C.J. Devall, T.D. Leininger, and M.E. Warren. District, Vicksburg, Miss. Sheviak, and D.L. Leopold, eds., Ecosystem 2000. Restoring bottomland hardwood [USFWS] U.S. Fish and Wildlife Service. 1986. Management: Rare Species and Significant th Natural Areas ecosystems in the lower Mississippi Alluvial Endangered and threatened wildlife and Habitats. Proceedings 15 Association Conference, Bulletin 471, New Valley. Journal of Forestry 98:10-16. plants; determination of endangered status York State Museum, Albany. Steyermark, C. 1984. Behind the Scenes. Mis- for Lindera melissifolia. Federal Register souri Botanical Garden, St. Louis. 51:27495-27500. Wright, R.D. 1990. Photosynthetic competence of an endangered shrub, Lindera melissifolia. Steyermark, J. 1949. Lindera melissaefolia. [USFWS] U.S. Fish and Wildlife Service.1993. Proceedings of the Arkansas Academy of Rhodora 608:153-162. Recovery plan for pondberry (Lindera me- Science 44:118-120. lissifolia). U.S. Fish and Wildlife Service, Torres, A.M., U. Diedenhofen, B.O. Bergh, and Wright, R.D. 1994. Sex ratio and success, an Atlanta, Ga. R.J. Knight. 1978. Enzyme polymorphisms assessment of Lindera melissifolia in Arkan- as genetic markers in the avocado. American [USFWS] U.S. Fish and Wildlife Service. 2012. sas. Proceedings of the Arkansas Academy Journal of Botany 65:134-139. Species profile for pondberry (Lindera me- of Science 48:230-233. Tucker, G.E. 1984. Status report on Lindera lissifolia). Available online
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