Fruit and seed dispersal of Salvia L. (Lamiaceae): a review of the evidence.
Intraspecific gene flow is the means by which populations of sexually reproducing species establish genetic structure, i.e. maintain genetic diversity while at the same time preserve species coherence (Bohonak, 1999; Lenormand, 2002; Eckert et al., 2008). Gene flow occurs naturally in two ways: the movement of haplotypes through pollen dispersal and the movement of zygotes through seed dispersal. Of those two processes, only seed dispersal has the ability to colonize new habitats, escape predation and competition, persist over potentially long periods, or regenerate populations following disturbances, droughts or killing frosts. Nowadays, botanists can measure and track gene flow with precision that was undreamt of a generation ago, but the mechanisms by which pollen and especially seeds move at various scales across the landscape are known with considerably less accuracy.
In the genus Salvia L. (Lamiaceae: Nepetoideae), pollination has received more attention than seed dispersal, in part, one supposes, because animal pollinators can be "caught in the act." Pollinators of Salvia are a host of birds, bees, flies, and moths (Ohashi, 2002; Wester & Classen-Bockhoff, 2006a, 2006b; Celep et al., 2014; Ott et al., 2016; Reith & Zona, 2016), although pollination studies are surprisingly few for a genus of nearly 1000 species (Classen-Bockhoff, 2003). In stark contrast, seed dispersal has attracted far less attention and has been noted, often as incidental observations, for very few species. The purpose of this review is to explore seed dispersal in the genus Salvia, to document the diverse modes of dispersal and to identify gaps in our knowledge of the processes by which species disperse.
Throughout this review, van der Pijl's (1982) terminology will be used. Examples are drawn from an extensive review of the literature, as well as the author's personal experience with species in the wild and in cultivation.
General Morphology of Salvia
Salvia species are woody shrubs, herbaceous perennials, or annuals. They range in size from small, creeping species <30 cm tall to large shrubs up to 3 m, as well as semi-scandent species. Habit plays a role in seed dispersal generally. For example, in wind dispersal, release height of the diaspore is a key factor of the dispersal equation, with diaspores released from tall plants traveling farther than those released from short plants (Howe & Smallwood, 1982; Willson & Traveset, 2000; Nathan & Katul, 2005; Thomson et al., 2011). Ant-mediated dispersal is more common among short-stature plants (Willson & Traveset, 2000).
Habitats of Salvia are diverse ranging from desert to dry shrubland and chaparral to deciduous woodland, pine-oak woodland, and submontane ever-wet forest. Habitat is also closely linked to seed dispersal. For example, dry habitats are favored by seed-harvesting ants that play a role in dispersal, and wind-dispersal is more effective in open habitats (Howe & Smallwood, 1982; van Rheede van Oudtshoorn & van Rooyen, 1999; Willson & Traveset, 2000)
The flowers of Salvia are bome in groups (verticillasters) or sometimes solitary either in the leaf axils or in inflorescences at the apices of branches. Each flower is borne on a short pedicel (<3 cm long). The calyx is tubular, two-lipped, with 3-5 lobes; the calyx persists throughout the life of the flower and fruit and may increase in size during fruit development. The corolla is also tubular and generally strongly two-lipped. The lower lip is usually 3-lobed, with the center lobe larger than the lateral lobes. The stamens of Salvia are two, epipetalous, often motile, and highly modified and distinctive at the level of subgenus (Classen-Bockhoff, 2003; Walker et al., 2015). The gynoecium comprises a superior ovary, a slender gynobasic style and a 2-lobed stigma. The ovary is bilocular, but each locule is subdivided into two chambers. Each chamber bears a single ovule. During fruit development, the calyx may remain open at its apex or it may close by the lips of the calyx pressing together. Upon maturity, the ovary is a smooth, dry, four-lobed, schizocarpic fruit that fragments into four, single-seeded mericarps (nutlets). The mericarps of Salvia are small, on the order of 0.5-4.0 mm long. The mericarps function as seeds and are sometimes called "seeds" in the horticultural, food science, or ecological literature. They are smooth and flattened ovoid, ellipsoid, or spheroid, sometimes three-sided (as a result of compression during development), usually without any appendages. The fruit coats of many species release mucilage upon contact with water (Hedge, 1970; Ryding, 2001).
Dispersal begins when the fruit (and sometimes the enclosing calyx) abscises from the mother plant. In many studies, this is called primary or phase 1 dispersal (Chambers & MacMahon, 1994; van Rheede van Oudtshoorn & van Rooyen, 1999; Wang & Smith, 2002). In many instances (e.g., epizoochory--see below), this is the only stage of dispersal, but in others, a secondary or phase 2 dispersal may occur after the fruit has fallen to the ground. The second phase may include transport by animals, wind, or water.
Anemochory is the dispersal of diaspores by wind. Anemochory has the potential to disperse diaspores farther than other modes of dispersal, given the appropriate habitat conditions, viz. open, unobstructed habitats such as steppes and plains (Willson & Traveset, 2000; Nathan et al., 2008). Extreme winds (i.e., cyclones) even have the potential for transporting diaspores across intercontinental or transoceanic distances (Sanmartin et al., 2007; Nathan et al., 2008), although plants have not evolved specific adaptations for extreme wind dispersal. Diaspores small enough--and resilient enough --to survive lofting into the upper atmosphere can achieve global distribution (Kellogg & Griffin 2006).
The mericarps of Salvia are small but larger than dust seeds or spores, so they are small enough to be transported by wind but unlikely to achieve long-distance dispersal except by extreme winds. Regardless of the size and terminal velocity of a Salvia mericarp, if it is released at a height at which it can be captured by wind flow, it will be dispersed by the wind (Thomson et al, 2011). Mericarps are usually without any appendages, such as wings or tufts of hairs found in other Lamiaceae (Bouman & Meeuse, 1992), which might assist in wind dispersal. The only species known to have appendages on their mericarps are Salvia arborescens and S. stobilanthoides (large shrubs from Hispaniola and Cuba, respectively) and S. albomaculata, a small shrub from southern Turkey. The mericarps of S. arborescens have a tail-like appendage that is 0.5-1.0 mm long (Fig. 1), about a third the total length of the mericarp (Zona et al., 2011). The role of these appendages in the dispersal of the mericarps is not known. They appear to be too small to affect the drag ratio and slow the descent of the mericarp in the air column, nor do they appear to position the mericarp on the soil surface prior to germination. Their function, if any, is unknown.
The cottony calyces of Salvia funerea, a shrub species endemic to the Mojave Desert of Nevada and California, USA, seem to be ideally adapted to catching the wind, although its dispersal biology has never been studied. The calyx is 4.6-6 mm long and densely covered in long, fluffy hairs and looking like small (ca. 10 mm diameter) balls of cotton (Fig. 2). One suspects the calyces detach and are blown or rolled about by the wind, but direct observations are lacking.
Salvia section Hymenosphace is native to arid or semi-arid regions of the Canary Islands, Central and Southwest Asia, Russia and southern Africa (Hedge, 1974; Dizkirici et al., 2015). It is characterized by accrescent calyces, which enlarge and become papery or inflated as the fruits mature (e.g., Salvia lanceolata of South Africa, Fig. 3). Such calyces may be well adapted for anemochory (Dizkirici et al., 2015), as they are in the Central Asiatic genus Hymenocrater (Ryding, 2001) or the shrub Scutellaria mexicana of the southwestern USA. Accrescent calyces may result in low-mass, high-drag structures that are readily dispersed by wind with the mericarps still enclosed. In the case of Salvia section Hymenosphace, experimental or observational data are, once again, lacking.
A remarkable case of anemochory in the genus Salvia is seen in S. aethiopis, a plant native to the Mediterranean region, southeastern Europe, and Central Asia. This plant grows as a biennial, producing a rosette of leaves in year one, followed by a large, candelabra-branched inflorescence in year two. Upon senescence and drying, the entire inflorescence snaps off near the base, along a predetermined zone of abscission (Roche, 1991), and disperses as a tumbleweed, scattering hundreds or even thousands of mericarps as it rolls. Mericarps of this species were accidentally introduced into the western USA as a contaminant of alfalfa seed, and the species is now considered to be a noxious weed in many of the western states (Roche. 1991). It is also spreading as a weed in Central Asia (Lazkov & Sennikov, 2014). This may be the only case of tumbleweed dispersal in Salvia; its close relatives (S. sclarea, S. candidissima, S. verbascifolia) are not known to be tumbleweeds.
Hydrochory is the dispersal by water, in which the diaspore floats on or is carried by water. The mericarps of some Salvia species are known to float, and they are small enough to be carried by flowing water (rivers or streams) or sheet flow as a result of heavy rainfall (rain wash). Hydrochory by heavy rain is especially important among desert plants (van Rheede van Oudtshoorn & van Rooyen, 1999). Hegland et al. (2001) speculated that the European S. pratensis might have mericarps spread by water, because the species is distributed along river banks and colonizes river dunes and sandbars. Their speculation was given additional weight by Praeger's report (cited by Ridley, 1930) that S. pratensis mericarps float up to eight days.
The results of my own experiments with mericarp floatation are shown in Table 1, in which mericarps are shown to float for at least 24 hours, long enough to be carried by water over a considerable distance. There is within- and between-species variation in buoyancy. The variability in this trait suggest that it may be subject to natural selection, although the heritability of the trait is unknown. The anatomical bases for mericarp buoyancy remain uninvestigated, but air pockets between the seed and pericarp are a likely cause. In species that produce mucilage, the mucilage itself may contribute to buoyancy.
A special case of water-dispersal involving rain drops is called ombrohydrochory. This is defined as primary dispersal by rain drops that activate ballistic mechanisms in the plant. In Salvia, ombrohydrochory occurs when raindrops strike the calyces containing the mericarps. The raindrop depresses the calyx briefly, and then the pedicel springs back to a neutral position, thereby ejecting the mericarps from the calyx. Brodie (1955) called this the "springboard mechanism." This mechanism has several advantages for the plant, viz. mericarps are protected until rainfall simultaneously disperses them and moistens the soil, preparing the seedbed (Walck & Hidayati, 2007). Brodie (1955) demonstrated this mechanism in the dispersal of Salvia lyrata, a small, woodland Salvia of eastern North America. His experimental investigation, involving water droplets falling from a height of 250 cm onto isolated infructescences clamped upright in the laboratory, found that mericarps were dispersed 50-200 cm from the source (Brodie, 1955).
My own experiments using Salvia roemeriana, a species endemic to Texan woodlands, found the springboard mechanism to be highly effective. Water drops (falling from a wash-bottle ca. 150 cm above the plants) dispersed mericarps 5-109 cm from the plant (mean = 35.1 cm; mode = 29 cm; n=75). These dispersal distances are likely to be somewhat greater than would occur in naturally growing plants because of the added height (16 cm) of the container (Thomson et al., 2011). Nevertheless, they demonstrate the functionality of the springboard mechanism in S. roemeriana. A similar experiment with S. coccinea found no springboard dispersal.
Epizoochory is dispersal on the outside of animals. Diaspores may be equipped with bristles, hooks, barbs, or sticky secretions for primary dispersal or they may be included in adhering mud (secondary dispersal). Epizoochory is inadvertent dispersal by animals when disapores adhere to fur, feathers or muddy feet. Even without bristles, hooks, or barbs, the mericarps of some Salvia species may be dispersed by animals, or have been shown to have the potential for epizoochorous dispersal.
Romermann et al. (2005) employed animal pelts and a mechanical shaking device to investigate the dispersal potential of various seeds. They combed mericarps into sheep and cow pelts and shook the pelts for one hour. Testing Salvia pratensis, they found 49.4% of the mericarps remained attached to the sheep's wool but only 2.3% remained in cattle hair. In both cases, they demonstrated the potential for Salvia mericarps to be dispersed by adhering to grazing animals. Their experiments were conducted with dry pelts and mericarps; adherence to wet pets might be even greater.
Many Salvia species are well known for their mucilaginous fruits (Hedge, 1970; Ryding, 2001). The mucilage has been assumed to be instrumental in adhering the mericarps to animals (Ridley, 1930; Melcher et al., 2000; Melendo et al., 2003; Sales et al., 2010), but direct, observational evidence for epizoochory of mucilaginous Salvia mericarps is lacking. Vazacova and Miinzbergova (2014) applied moistened mericarps of Salvia aegyptiaca and S. canariensis to the feathers of captive, domesticated pigeons and found that the mucilage glued the mericarps to the feathers for a time long enough, in theory, for a bird to fly from mainland Africa to the nearest island of the Canary Archipelago.
The possibility exists that a mucilaginous mericarp might adhere to a fallen leaf, which might then function like a wing for wind dispersal, but this mode of dispersal seems highly unlikely and certainly not typical of a species (van Rheede van Oudtshoorn & van Rooyen, 1999). Mucilage may have functions other than adhering a diaspore to an animal; the possible functions of mucilage include: expediting seed hydration, regulating seed dormancy, and prevention of seed movement (antitelechory) or predation by adherence to substrate (Garcia-Fayos et al, 2010; Kreitschitz, 2009, 2012; Western, 2012; Yang et al., 2012a, 2012b).
The antitelechorous function of Salvia mucilage has been addressed experimentally in two studies. In the first, Fuller and Hay (1983) examined Salvia columbariae and found that mericarps encrusted with sand (by virtue of the sticky mucilage) escaped predation from invertebrate and vertebrate granivores. Adhering sand grains decreased seed predation by 25% for heteromyid rodents, 94% for ants, and 77% for diurnal granivores (birds and ground squirrels). In the second study, Engelbrecht and GarciaFayos (2012) found that mericarps of S. rosmarinus (as Rosmarinus officinalis) adhering to bare soil escaped removal by ants 50% of the time, whereas only 0-20% of loose mericarps escaped predation. In both cases, mucilage functioned not as a means of epizoochory but rather as a means of avoiding predation by granivores.
Although the smooth mericarps of Salvia lack bristles, hooks or other means of attaching to animals, the calyces of some species readily abscise at fruit maturity and are richly endowed with hooks or sticky trichomes, which can adhere the calyx--and enclosed fruit--to passing animals, including people. Salvia madrensis (Fig. 4), S. occidentalis and S. caymenensis (Fig. 5) are species with sticky calyces that aid in epizoochorous dispersal (S. Zona, pers. obs.), and S. glutinosa and S. pratensis are believed to be dispersed similarly (Ridley, 1930; Fahn & Werker, 1972; Hegland et al., 2001). In S. caymensis the calyces are covered in long, sticky, capitate-glandular trichomes, as well as short, hooked, uniseriate trichomes (Fig. 5) that securely attach the calyces to hair and clothing (S. Zona, pers. obs.) and likely also to pelage and plumage. In other words, it has chemical and physical means by which it can hitch a ride on an animal. Nevertheless, direct evidence of epizoochory of Salvia calyces under natural conditions is unavailable. Animal grooming behavior will determine how long --and how far--a sticky calyx will remain attached.
Carlquist and Pauly (1985) investigated the potential of the hooks on the calyces of Salvia mellifera to function in epizoochory (Fig. 6). Their experiments used artificial fabrics that mimicked sheep's wool and cowhide and a mechanical shaking device. Their findings suggested that 12-20% of the calyces remained attached to the fabrics after 20 seconds of vigorous shaking. Curiously, the wool-like fabric was less good at entangling the hooked calyces of S. mellifera than was the hide-like fabric. While this experimental investigation was not a perfect mimic of natural conditions, it clearly demonstrated the potential of S. mellifera calyces to attach to animals and the different dispersal potentials of animals of various pelage.
Synzoochory is when animals intentionally transport propagative material, for example, when birds collect mosses for nesting material or when animals cache seeds for later consumption. A subcategory of synzoochory is mynnecochory, dispersal by ants. Most myrmechorous diaspores have a lipid-rich structure, such as an elaiosome, which is the food item desired by the ant; the attached seed is just ballast. Salvia mericarps lack elaiosomes. Nevertheless, granivorous ants, which transport mericarps to the nest for later consumption, likely play a role in Salvia seed dispersal. The granivorous red harvester ant, Pogonomyrmex barbatus, selectively predates the mericarps of Salvia texana and in doing so influences the composition of grass and forb communities in the Edwards Plateau, Texas (Nicolai, 2005).
Buisson and Dutoit (2004) trapped ants carrying mericarps of Salvia verbenaca in southeastern France. This is strong evidence for myrmecochory, although it is not clear whether the traps (5-cm diameter, fluid-filled containers) were open to seed rain, as the authors also found mericarps of this species in their seed rain traps (sticky traps). Engelbrecht and Garcia-Fayos (2012) observed that granivorous ants were so eager to harvest mericarps from Salvia rosmarinus (as Rosmarinus officinalis) that they would cut the entire calyx (with enclosed faut) from the plant and transport the entire structure toward the nest. The authors noted that it is likely that some mericarps fall from the calyx during transport and may escape predation. The authors' observations are unequivocal evidence for myrmecochory. A similarly strong case for myrmecochory is drawn from the work of Steinberger et al. (1991). In their analysis of the chaff piles (middens) of harvester ants (Messor ebeninus and M. arenarias) in Israel, they found calyces with enclosed mericarps of Salvia lanigera. While this is evidence that ants transport the mericarps, it is not known whether the mericarps can germinate and establish in the chaff pile microenvironment. Harvester ants also predate the mericarps of S. apiana and S. mellifera in California and may contribute to their dispersal (Montalvo, 2004; Montalvo & McMillan, 2004).
Endozoochory is dispersal of diaspores in the digestive tracts of animals. Typically, endozoorchorous taxa are plants with fleshy, nutritious fruits, which reward dispersers, such as birds, bats and non-flying mammals, as well as reptiles and fish. Only a very few members of the Lamiaceae have evolved fleshy, animal-attracting fruits (or fruits plus accessory structures), but no Salvia has done so. Nevertheless, there is evidence that mericarps ingested along with foliage by large browsing mammals may survive passage through the gut and germinate. Salvia chamelaeagnea, a mesophyll shrub from the Northern and Western Cape of South Africa, was said by Midoko-Iponga et al. (2005) to be "dung-dispersed." No other information on this species' dispersal ecology was found.
A study by Bonn (2004) found that seeds of S. pratensis survived passage through sheep's gut better than cattle gut--but only at very low rates. Nevertheless, even low rates of dispersal can have a positive effect on species fitness (Nathan et al., 2008). Studies that suggest some species of Salvia may be dispersed by large browsing animals fit the foliage-is-the-fruit hypothesis of Janzen (1984), although van der Pijl (1982) called this accidental dispersal. The resistance of the mericarp to digestion, the ability of the seed to germinate, and the establishment of the seedling are all subject to natural selection, even when dispersal is accidental.
The possibility of bird dispersal of several Angiosperm species, including Salvia canariensis, was investigated experimentally by Vazacova and Munzbergova (2013). They found a small number of mericarps survived ingestion and gut passage in a domestic pigeon, a bird normally regarded as granivorous and a seed predator. Salvia canariensis mericarps were viable after passage through the bird; the authors suggested that the mucilage produced by the fruit provided some protection from the digestive system of the bird. The possibility that birds can occasionally disperse viable Salvia mericarps in their guts offers an explanation for the extensive present-day distribution of Salvia, particularly on oceanic islands, such as the Canary Archipelago.
Autochory is dispersal by the plant itself, using no outside forces in moving the diaspore. This category includes the spectacular explosive mechanisms of many Fabaceae, Acanthaceae, Impatiens, Oxalis, etc. These were termed "active ballists" by van der Pijl (1982). Salvia does not possess any kind of explosive mechanism for dispersal and falls into van der Pijl's (1982) "passive ballists" category. These plants shed their diaspores by the action of wind or passing animals, and thus rely to a slight extent on an outside force. This mode of dispersal is sometimes called semachory or boleochory. In theory, Salvia stems swayed by the wind might cast their mericarps farther than if the mericarps simply dropped to the ground (see barochory, below). In practice, this mechanism of dispersal has never been observed or even simulated experimentally. The theoretical line between autochory and barochory (see below) is both fine and faint.
Diacon-Bolli et al. (2013) acquired seed-trap evidence of short distance ([less than or equal to] 1 m) dispersal of S. pratensis in calcareous grasslands in Switzerland possibly as the result of autochory, but they also found a small number of mericarps of S. pratensis in an arable field up to 40 m from the adjacent grassland source population. It is doubtful that S. pratensis could have dispersed up to 40 m by autochory alone. It is more likely that S. pratensis dispersed into the arable field via epizoochory or by wind dispersal. The experimental design did not control for the possibility of wild animals. Buisson and Dutoit (2004) also reported mericarps of S. verbenaca in sticky traps laid out along transects some distance from the source population, but there is no indication that they controlled for possible wind dispersal. The same can be said for S. apiana mericarps trapped in southern California grasslands up to 30 m from the source population (DeSimone & Zedier, 2001). Ramirez-Marcial et al. (1992) found mericarps of S. karwinskii in seed traps, but the dispersal mode, whether autochory or anemochory. was not investigated.
Barochory refers to dropping the seed or fruit directly below the plant; in other words, plants with no apparent dispersal mechanism, other than gravity, are said to exhibit barochory. In the case of Salvia, barochory is very common; many authors note that Salvia species lack any means of dispersal (Navarroa et al., 2009; Vargas et al, 2012; Cortes-Flores et al., 2013; Zamora & Matias, 2014). Many species allow their mericarps simply to drop out of the calyx and onto the soil below the plant. Such a system would appear to put the mericarps at increased risk of predation from seed-feeding animals and competition from the mother plant and siblings, the very raison d'etre of the predator avoidance or escape hypothesis of dispersal (Howe & Smallwood, 1982; Hyatt et al., 2003).
In some cases, barochory is thought to be the first phase in a system that exploits two or more dispersal mechanisms. For example, barochory (primary dispersal) could be followed by myrmecochory or hydrochory (secondary dispersal). Some species of Salvia (e.g., S. connivens and S. rosei) mature their fruits in closed calyces (J. G. Gonzalez-Gallegos, pers. comm.). The dried, bilabiate calyx, with its lips pressed together, falls from the parent plant with the mericarps enclosed. This primary dispersal may be followed by secondary dispersal by water, as floatation by these closed calyces is very likely but has not been tested experimentally. Corsi and Bottega (1999) noted that, despite long periods of observation, no animal approached the fallen mericarps of Salvia officinalis, which otherwise simply laid on the ground beneath the parent plant. It appears that the mericarps of some Salvia species simply fall to the ground.
Salvia mexicana and S. tiliifolia mericarps were captured in seed rain traps in Mexico (Martinez-Orea et al., 2014); similarly, Salvia japonica was found in the margins of modern, consolidated rice paddies in Japan, some distance from possible source vegetation on the margins of traditionally managed rice paddies (Matsumura & Takeda, 2010). In both Mexican and Japanese cases, the authors indicated that the dispersal mechanisms for these species were barochory. However, secondary amenochory and hydrochory cannot be ruled out from these accounts.
A special case of barochory is found in the dispersal mechanism of Salvia viridis (syn. S. hormium), a perennial shrub from the Middle East. It is dependent on activation by water, although it is not hydrochory, as water is not transporting the diaspore. In Salvia viridis, both the pedicel and the calyx exhibit hygroscopic movements (Fahn & Werker, 1972). In the dry condition, the persistent calyx is pointed downward and the inner epidermis of the calyx contracts, constricting the calyx tube and pulling together the two lips of the calyx. Upon wetting, the pedicel reorients the calyx to the horizontal position, and the calyx "relaxes" to open and release the mericarps. This mechanism protects the mericarps prior to dispersal and releases them when moisture is present, which is crucial to seed germination and establishment. Other species from arid North Africa, viz. S. algeriensis and 5. mouretii, along with S. barrelieri from Spain and North Africa, have calyces that are deflexed downward in fruit (Hedge, 1974), but it is not known if they exhibit hygroscopic movement in association with mericarp release.
There are other examples of mechanisms that retard the release of mericarps, either to extend the time period during which mericarps are released or to hold the mericarps until another dispersal mechanism is initiated (e.g., the tumbleweed dispersal of S. aethiopis or epizoochory of S. caymanensis). Generally, mericarps are prevented from dispersing by the lobes of the calyx, which can press together, either bilaterally or dorsoventrally, depending on the species. Another mechanism that retards dispersal is a collar of trichomes in the interior of the calyx tube. In S. miltiorrhiza, a species from moist woodlands of China, villous trichomes, up to 3 mm long, form a dense ring half-way up the calyx tube (Fig. 7). A similar mechanism--stiff hairs inside the calyx--is found in Salvia sect. Salvastrum of Texas and adjacent areas. How the mericarps escape their trichome prison is not known.
There is a small body of evidence that mericarps of Salvia, despite being rather similar in morphology throughout the genus, disperse by various means, including wind, animals, floatation, and raindrops, or simply by gravity. Different species have specialized morphological adaptations for dispersal, although many have no visible adaptations at all. Even species with no special adaptions for dispersal, when examined by ecologists, have been found to disperse their mericarps short distances (up to tens of meters) from parent plants. The diversity of dispersal mechanisms in Salvia parallels the diversity found throughout the remainder of the Lamiaceae (Bouman & Meeuse, 1992).
This literature review identifies large gaps in our knowledge of Salvia mericarp dispersal. A few published studies address seed dispersal as part of broader ecological studies, but only a very few focus specifically on Salvia dispersal. The state of our understanding of Salvia dispersal often relies on anecdotal evidence or inferences from morphology, much as our understanding of Salvia pollination biology did some twenty or more years ago. Even the most basic questions--Does the fruit mature in an open or closed calyx? Do mericarps fall out of the calyx, or does the calyx abscise with the mericarps still inside?--are not known for most species in the genus, and yet the answers have significant dispersal implications!
Knowledge of dispersal mechanisms plays a pivotal role in managing species of conservation concern. For example, Salvia caymanensis is critically endangered in its native habitat (the Cayman Islands), where it is short-lived perennial restricted to ruderal, disturbed habitats (Clubbe et al., 2010). In order to persist over time, it must rely on a very long-lived seed bank or, more likely, frequent dispersal to new, suitable habitats via epizoochory, although the animals that disperse this species are unknown. Conserving this Salvia in situ may require measures to conserve the animals that disperse its mericarps.
Global climate change is likely to cause many species to migrate (Watkinson & Gill, 2002; Feeley et al., 2012; Duque et al., 2015). Knowledge of dispersal rates and distances for vulnerable Salvia species will allow biologists to model and predict their response to climate change. We do not yet know whether vulnerable Salvia species, e.g. coastal or tropical montane species, will be able to migrate rapidly enough to stay abreast of changing climates and their effects on habitats.
Habitat restoration is an activity in which knowledge of plant dispersal mechanisms is an important component. Salvia species are sometimes a part of the restoration target (Buisson & Dutoit, 2004; Hegland et al., 2001; Diacon-Bolli et al., 2013) or incidental to the restoration, appearing in restored habitats on their own accord via dispersal. For example, in studying the value of grazing animal exclosures in restoring degraded drylands in Tigray, Ethiopia, Birhane et al. (2007) found Salvia dianthera (as Meriandra bengalensis) appearing within exclosures even though its diaspores were not found in the seed banks of soils within or outside exclosures. We are left to conclude that this species dispersed on its own accord into the exclosures, where protected from animals, it established and grew. Kasowska and Koszelnik-Leszek (2014) reported that S. pratensis appeared spontaneously on serpentine mine tailings in Poland; the authors attributed the spccies' appearance to dispersal by wind. Other species (e.g., Salvia finticosa) regenerated after fire from a persistent soil seed bank (Ne'eman & Dafni, 1999). The distinction between those species that recolonize via dispersal and those that recolonize via the soil seed bank has obvious implications in habitat management and restoration.
Some species of Salvia are invasive weeds (e.g., S. aethiops), and clearly dispersal mechanism is correlated with invasive history and invasive potential (Davies & Sheley, 2007; Skarpaas & Shea, 2007). For example, Salvia glutinosa, an Old World species, has been found naturalized in New York, USA, although is mode of dispersal as an introduced weed is in need of further study (Tabak, 2011). Understanding the dispersal mechanisms of Salvia species will lead to more accurate risk assessments and management (Crossman et al, 2008), especially since the internet facilitates international commerce in plants and seeds (Giltrap et al., 2009), and more Salvia species are entering the horticultural trade than ever before.
The retention of mericarps is an important characteristic of some land races of chia, Salvia hispanico. This species, domesticated in Mexico in pre-Columbian times, normally releases its mericarps through an open-mouthed calyx, but fully domesticated cultivars retain their mericarps in closed calyces (Cahill, 2005; Hernandez Gomez & Miranda Colin, 2008). The genetic basis for this character trait is unknown, but it is clearly variable and subject to human selection.
There are many phytogeographic puzzles in the genus Salvia that might be solved with a better understanding of dispersal. Across Salvia subgenus Calosphace, molecular evidence identified numerous interclade, phylogeographic divisions that suggest past dispersal events (Jenks et al., 2013). For example, taxa representing sections Blakea of Mexico/Central America, the monotypic Standlyeana also of Mexico/ Central America, and Hastatae of the Andes form a strongly supported clade. On another branch of the tree, species of the Andean section Corrugatae are embedded in a clade of Mexican/Central American taxa. For each case, the authors suggested a single, founding dispersal event from Mexico/Central America to South America (Jenks et al, 2013). Similarly, recent molecular phylogenetic study of Caribbean species of Salvia suggested that one clade of Hispaniolan taxa was derived from ancestors in the northern Andes and thus implicated historic dispersal from the Andes in the evolution of Hispaniolan endemic Salvia (Zona et al., 2016).
Dispersal is implicated at the specific level as well. For example, Salvia tubifera has a saltational distribution in Mexico: it is abundant in southern Mexico and adjacent Central America, but farther to the north, it is found in southern Guerrero, a single site in Jalisco, and once again in Durango (J. G. Gonzalez-Gallegos, pers. comm.). Its ability to hop across apparently suitable habitat throughout much of Mexico suggests a long-distance dispersal mechanism of, perhaps, birds. A similar example is Salvia brandegeei, a species found on Santa Rosa, the second largest of the Channel Islands of California, and again over 350 km to the southeast, on the mainland in Baja California, Mexico. Recent investigations have linked the prevailing direction of wind (from the northwest to the southeast) to colonization via wind dispersal within the Channel Islands (Riley & McGlaughlin, 2016; Riley et al., 2016); could the same process explain the presence of S. brandegeei on mainland Baja California?
In order to fill the gaps in our knowledge of Salvia dispersal, we surely need more natural history observations and studies of Salvia species in situ. More autecology studies also are greatly desired. In addition, experimental studies of mericarp mucilage production (myxocarpy), mericarp/calyx buoyancy in air and water, and mericarp/calyx feeding trials with animals, including granivorous ants and birds, will provide much-needed data that can inform and explain field observations. Do species that disperse their calyces with the mericarps inside have stickier calyces compared with those that retain their calyces? If so, we may be able to conclude that sticky glandular hairs on the calyx function more in dispersal than in deterring herbivores (Bottega & Corsi, 2000) and that selection for dispersal, rather than defense, has shaped the evolution of calyx glandular hairs.
Salvia dispersal studies have focused on meadow and grassland ecosystems, deserts and dry shrublands, and some woodland habitats, but Salvia species are found in many other kinds of ecosystems. Glaringly absent are studies of dispersal in high-elevation, Neotropical forests and the temperate deciduous woodlands of Eastern Asia. These habitat gaps also correspond to geographic gaps in the study of Salvia. Most of the information on Salvia dispersal comes from Europe and Israel, and some additional data from California and eastern North America. Evidence is lacking from other important centers of Salvia diversity, viz. Eastern Asia, southern Africa, eastern South America, the northern Andes, Mexico and the West Indies. Botanists, ecologists and field biologists in these regions are encouraged to study the dispersal of Salvia-, they are bound to be rewarded with findings that will fill in many of the gaps in our understanding of this large, widespread and fascinating genus.
Acknowledgments I thank Dr. Jesus G. Gonzalez-Gallegos for sharing his insights into the biology of Salvia species in Mexico. This is contribution 333 to the FIU Tropical Biology Series.
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Scott Zona (1,2)
(1) Department of Biological Sciences & International Center for Tropical Botany, Florida International University, 11200 SW 8 St., Miami, FL 33199, USA
(2) Author for Correspondence; e-mail: firstname.lastname@example.org
Published online: 25 April 2017
Caption: Fig. 1. The mericarps of Salvia arborescens have tail-like appendages. Scale divisions are in mm
Caption: Fig. 2. Cotton-ball calyces of Salvia fimierea are likely transported by the wind. Photo by Nhu Nguyen, used with permission
Caption: Fig. 3. Salvia laceolata showing the enlarged, papery calyces that are typical for section Hymenosphace. Photo courtesy of Daniel L. Nickrent. Phytolmages, available from: http://www.phytoimages.siu.edu
Caption: Fig. 4. Salvia madrensis calyces attached to socks by means of sticky glandular trichomes
Caption: Fig. 5. Photomicrograph of Salvia caymanensis showing glandular trichomes. Scale divisions arc in mm
Caption: Fig. 6. Salvia mellifera has calyces that detach and cling to animals. Photo by Marisa Evans, used with permission
Caption: Fig. 7. Longitudinal section through the calyx, ovary and nectary of Salvia miltiorrhiza showing the stiff ring of trichomes that occludes the throat of the calyx. Note also the sticky glandular trichomes on the outside of the calyx. Scale bar = 1 mm
Table 1. Experiments in Salvia mericarp floatation Percent (%) of floating after species n 6 hrs 24 hrs mucilaginous S. apiana Jeps. 40 100 73 yes S. carduacea Benth. 40 50 25 yes S. caymanensis Millsp. & Ulinc 20 5 0 yes S. coccinea Buc'hoz ex Etl. 50 76 62 yes S. columbariae Benth. 40 8 8 yes S. farinacea Benth. 50 18 12 yes S. hierosolvmitana Boiss. 20 90 65 yes S. hispanico L. 40 0 0 yes S. lyrata L. 50 52 6 yes S. miltiorrhiza Bunge 30 10 3 yes S. miniata Fernald 30 70 70 no S. officinalis L. 40 60 58 no S. purpurea Cav. 50 90 78 yes S. roemeriana Scheele 40 75 8 yes S. texana (Scheele) Torr. 30 23 7 yes S. verticillata L. 40 58 48 no S. whitehousei Alziar 30 40 27 yes Each experiment consisted of 10 mericarps in 15 ml water, rcplicated according to mericarp availability. Seed viability post-floatation was not tested, but samples were taken from seed lots less than 6 months old and known to be viable
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|Date:||Jun 1, 2017|
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