Differences between life cycles, particularly phenological shifts, constitute an important basis for taxonomic distinctions in Arceuthobium. Here we discuss the salient features of the dwarf mistletoe life cycle, excluding the more detailed aspects of sexual reproduction, which are treated separately in chapter 3. Shoots, flowers, and fruits of Arceuthobium are illustrated in figures 2.1, 2.2, 2.3 and 2.4. The critical features of the life cycle of a representative species (A. americanum) are shown in figure 2.5.
The life cycles of the following species have been studied in some detail:
Various features of the life cycle are illustrated photographically: pistillate plant with mature fruit and characteristic swelling at the point of infection (fig. 2.6); mature staminate flowers at anthesis with moistened nectaries (fig. 2.7); pistillate flowers at anthesis with pollination droplets (fig. 2.8); mature fruit ready for dispersal (fig. 2.9); explosive dispersal of the seed (fig. 2.4); the dispersed seed sticking to a needle by means of its viscin coating (fig.2.10A); the dispersed seed sliding down the needle in the hygroscopically expanded viscin mass (fig. 2.10B); the seed and viscin at the base of a needle (fig. 2.10C); the germinated seed and elongated hypocotyl that has developed a holdfast from which infection can occur (fig. 2.11); the microscopic "penetration wedge" entering the host tissue (fig. 2.12); and young shoots emerging from the swollen tissue of a new infection (fig. 2.13).
Our discussion of the dwarf mistletoe life cycle begins with the seed. The fruit normally contains a single seed with one embryo, but fruits may rarely contain two seeds or a single seed with two embryos (Weir 1914, Hawksworth 1961b). Dwarf mistletoes possess one of the most effective hydrostatically controlled, explosive mechanisms of seed dispersal known in flowering plants (fig. 2.4) (Hinds and others 1963, Hinds and others 1965; van der Pijl 1972). The only exception to this mode of dispersal among the dwarf mistletoes is exhibited by Arceuthobium verticilliflorum, which has the largest seeds in the genus (11 x 6 mm). In fact, these seeds are greater than twice the size of those of any other dwarf mistletoes. Fruits of A. verticilliflorum exhibit a weak explosive mechanism that accomplishes little more than removing the pericarp and exposing the seed. Seeds of A. verticilliflorum are undoubtedly dispersed primarily by birds.
Among temperate species of dwarf mistletoes, seeds are explosively discharged during late summer at velocities of about 27 m per second (Hinds and others 1963) (fig. 2.4). Maximum dispersal distance is about 16 m, but dispersal distances of 10 m or less are more typical. Most seeds are intercepted within 2 to 4 m by host needles. Seeds have a viscous coating (viscin) that readily adheres to any object they strike, especially conifer needles (fig. 2.10A) (Roth 1959, Hawksworth 1965b). Intercepted seeds usually remain on the needles until the first fall rain wets the hygroscopic viscin (fig. 2.10B). Gravity then pulls the well-lubricated seed to the base of an upright needle (fig. 2.10C). As the viscin dries, the seed is cemented to the shoot surface. Seeds intercepted by downward-pointing needles generally fall to lower branches or to the ground (Shaw and Loopstra 1991). To achieve infection, seeds must lodge on shoot segments usually less than 5 years old; only this portion of the host can be considered a "safe-site," i.e., a place where a seed can germinate and establish an infection.
Studies of three species of dwarf mistletoes indicate that about 40% of dispersed seeds are intercepted by trees (Hawksworth 1965b, Smith 1985). Seed interception rates, however, are highly variable and depend on stand structure and composition, position of the dwarf mistletoe on the host, and needle characteristics of the host tree. For example, an adjoining tree within 2 to 3 m of an infected host will intercept about 90% of the seeds dispersed in its direction. From an infection site on the outer edge of a host crown, about 70% of discharged seeds will be dispersed outward, and the remaining seeds will be discharged inward. Only 40% of the outwardly dispersed seeds will escape from the host crown. Dwarf mistletoe shoots located closer to the interior of the crown will disperse only 20 to 30% of their seeds out of the crown (Smith 1985). Because few seeds escape the host crown, secondary infection is common, and intensification proceeds rapidly once a host tree becomes infected.
Many intercepted seeds are not deposited at safe-sites, and a high proportion of those that do arrive at safe-sites are lost to disease, predation, or removal by rain. Less than 10% of seeds reach safe-sites (Hawksworth 1965b), and less than 5% of these establish new infections (Hawksworth 1961b, Wicker 1967a).
Within infested stands in Colorado, Arceuthobium americanum and A. vaginatum subsp. cryptopodum produce 0.9 to 1.3 million dwarf mistletoe seeds per hectare (Hawksworth 1965b). Smith (1973) estimated that a single Tsuga heterophylla tree infected by A. tsugense produced 73,000 dwarf mistletoe seeds annually, and Wicker (1967a) calculated that A. campylopodum on Pinus ponderosa produced an average of 32,000 (range 800 to 2.2 million) seeds per tree.
The large number of seeds produced compensates for the high proportional loss of seeds before infection. Consequently, explosive dispersal is a sufficiently effective mechanism for short distances so that dwarf mistletoes can spread rapidly within infested stands (Hawksworth 1965a). Beyond the explosive range of the dwarf mistletoe fruits, however, animal vectors are required for dispersal (chapter 8).
The seeds of most dwarf mistletoes have few characteristics that are typical for seeds of flowering plants. Because there are no true ovules in either the Viscaceae or Loranthaceae, there are no testa and consequently no true "seeds." The "seed" is an embryo embedded in a chlorophyllous endosperm surrounded by a layer of viscin. The embryo is green, rod-shaped, and only several millimeters long; and it possesses a meristematic radicular apex without a root cap. The cotyledons are vestigial.
Germination consists of little more than the initiation of meristematic activity at the radicular apex. The role of moisture in germination varies among species. Germination is virtually independent of humidity in Arceuthobium abietinum (Scharpf 1970), but free water greatly enhances embryo growth in A. pusillum (Bonga 1972). In temperate zones, seeds typically germinate with the onset of higher temperatures in the spring. Optimal embryo elongation occurs from 15 to 20° C (Gill and Hawksworth 1961, Scharpf 1970). Light significantly enhances germination of mistletoe seeds in general (Lamont 1983a) and that of several dwarf mistletoe species in particular (Scharpf 1970, Wicker 1974a).
Field germinability in excess of 90% is reported for Arceuthobium americanum, A. vaginatum subsp. cryptopodum (Hawksworth 1965a), and A. abietinum (Scharpf and Parmeter 1982). For other dwarf mistletoes, however, field germinability is apparently much lower: A. pusillum—7% (Baker and others 1979) to 25% (French 1968); A. tsugense—45% (Carpenter and others 1979), 3% (Smith 1965), 23% (Smith 1985), to 38% (Shaw and Loopstra 1991). Environmental factors undoubtedly play a strong role in germination. D. L. Nickrent (personal communication) indicates that mature seeds typically exhibit high percentages of germination under laboratory conditions.
The time of germination of many species is poorly known, but most temperate species germinate in the spring following fall dispersal. However, a few species (notably Arceuthobium vaginatum subsp. cryptopodum and A. guatemalense) germinate immediately after seed dispersal in the autumn. Seeds of some tropical Mexican and Central American species may also germinate soon after dispersal at the end of the wet season (late August to early September).
Dormancy in the traditional sense does not exist in dwarf mistletoes. Seeds stored under optimal conditions retained 58% germinability for 15 months (Knutson 1969, 1984); under laboratory conditions, some seeds remained viable up to 4 years (Beckman and Roth 1968). In the field, however, there is no evidence that seeds survive longer than the season following dispersal. Likewise, traditional "after-ripening" is not characteristic of dwarf mistletoe seeds (Scharpf 1970, Lamont 1983a), although varying periods of stratification did enhance germination for some species (Wicker 1965, Holmes and others 1968). Substrate appears to play no role in germination.
Perhaps the most unusual feature of all viscaceous seeds is the chlorophyllous endosperm. Although the embryo is also chlorophyllous, this condition is common for plant embryos. The growing hypocotyl possesses stomata, and the seed is photosynthetic (Tocher and others 1984). Lamont (1983a) suggests that simple sugars produced photosynthetically are a more efficient source of energy for radicular growth than the complex carbohydrates typical of storage endosperm. The autotrophic capability of germinating seeds of dwarf mistletoes undoubtedly increases their longevity beyond the availability of stored nutrients and, therefore, increases the likelihood of infection. Of course, growth of the hypocotyl is ultimately limited, and only those seeds that germinate within 5 mm of susceptible young shoots are likely to cause infection.
Infection is the equivalent of seedling establishment among terrestrial flowering plants. Successful infection by a dwarf mistletoe requires penetration of the host cortex by a growing embryo and development of an endophytic system. For most combinations of the host and dwarf mistletoe, infection can take place only through young stem tissues, usually a segment less than 5 years old. Arceuthobium americanum, however, can penetrate through the thin, chlorophyllous bark of Pinus contorta branches as old as 60 years (Hawksworth 1954).
The growing radicular apex has a unique combination of tropistic responses that promote infection. The radicular apex typically grows toward the low light intensities that characterize the surface of the host (negative phototropism), irrespective of the gravitational considerations (neutral geotropism). When the radicular apex encounters an obstruction such as a needle base, it responds (positive thigmotropism) by developing a rounded structure termed a "holdfast" (Bonga 1969b) (fig. 2.11).
The center of the holdfast then develops a region of intense meristematic activity known as a "penetration wedge" (fig. 2.12). The penetration wedge grows into the host cortex by exerting mechanical pressure (Scharpf 1963, Scharpf and Parmeter 1967). After the penetration wedge has entered the cortex, a rootlike endophytic system ramifies throughout the bark. Those portions of the endophytic system that subsequently become embedded in successive layers of xylem are described as "sinkers" (chapter 11).
Once infection is established, an incubation period of 2 to 5 years elapses before young shoots appear (fig. 2.13; see also 16.112 and table 2.1). A swelling at the point of infection usually precedes shoot production by a year or more. The incubation period or latency between infection and appearance of shoots (or swellings) varies by species of dwarf mistletoe, species of host, and various environmental factors. For example, in British Columbia, about half of the infections of Arceuthobium tsugense produced shoots in the second year after infection and an additional third produced shoots the following year (Smith 1971), whereas the incubation period extends 3 to 6 years in Alaska (Shaw and Loopstra 1991). The incubation period in other species lasts for 4 years—A. pusillum (Baker and others 1981); for 6 years—A. campylopodum (Wagener 1962) and A. tsugense (Shaw and Loopstra 1991); for 8 years—A. americanum (Hawksworth and Johnson 1989a) and A. vaginatum subsp. cryptopodum (Hawksworth 1961a); for 10 years—A. abietinum f. sp. magnificae (Scharpf and Parmeter 1982); or as long as 12 years—A. abietinum f. sp. concoloris (Scharpf and Parmeter 1982). Dwarf mistletoe plants begin to flower 1 or 2 years after the initial shoots appear.
Dwarf mistletoes are typically parasites on branches or main stems of conifer trees, but they rarely occur on roots. Known instances of root parasitism include Arceuthobium occidentale on digger pine in California (reported by Scharpf in Kuijt 1969a), A. globosum subsp. grandicaule on pines in Guatemala (Steyermark MICH 36940 and our observations in central Mexico), A. vaginatum subsp. vaginatum on Pinus hartwegii in Mexico (Vasquez 1991), and A. vaginatum subsp. cryptopodum on ponderosa pine in Arizona (our observations) (fig. 2.14). These cases are abnormal, however, and result from vegetative growth into the roots from infections that originated on a main stem near the root collar. This phenomenon is not comparable to root parasitism in typical terrestrial mistletoes of the Loranthaceae (Gaiadendron, Nuytsia, Atkinsonia), where infection takes place initially through the roots (Kuijt 1969a).
Meiosis may either occur immediately before flower production (direct flowering) or approximately 5 to 8 months before anthesis (indirect flowering) (Wiens 1968). Most species exhibit definite annual flowering periods, but a few tropical species (e.g., Arceuthobium aureum subsp. aureum) appear to flower continuously throughout the year. Arceuthobium abietis-religiosae and A. nigrum (both species found in Mexico) display two distinct flowering periods, and A. hawksworthii (found in Belize) may produce three flower crops annually (Wiens and Shaw 1994). Arceuthobium juniperi-procerae (found in East Africa) appears to produce several discrete flower crops annually. Flowering may occur as early as February or March (e.g., by A. globosum) or as late as November-January (e.g., by A. occidentale). For a given species and locality, flowering usually lasts 4 to 6 weeks, but most of the pollen is dispersed within a shorter, 2– to 3–week period.
The staminate flowers and terminal portions of the shoots are usually shed a few weeks after anthesis. However, the entire staminate flowering spikes of Arceuthobium verticilliflorum dehisce following anthesis. Individual shoots of most species produce crops of flowers over several successive years; A. pusillum produces a single crop. There were early reports that dwarf mistletoe shoots die after fruits mature (Peirce 1905, Korstian and Long 1922), but this is not typical of species other than the diminutive A. pusillum and perhaps A. minutissimum. Most shoots produce at least two successive crops of flowers. In Colorado, individual pistillate shoots of both A. americanum and A. vaginatum subsp. cryptopodum have produced successive fruit crops for 5 years (making these shoots at least 7 years old). Kuijt (1970) also reports that several species have relatively long-lived shoots.
The time required from pollination to fruit maturity varies considerably. Arceuthobium pusillum and perhaps some tropical species (e.g., A. juniperi-procerae) require about 5 months for fruit to develop. Fruit maturation may occur in about 4 months in A. hawksworthii from Belize. Most temperate species need one or more years for fruit to mature; A. gillii requires 19 months. The minimum time from infection to initial seed production averages 6 years for A. americanum (Hawksworth and Johnson 1989a) and 7 to 8 years for A. vaginatum subsp. cryptopodum (Hawksworth 1961a).