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Age of Maturity and Life Span in Herbaceous, Polycarpic Perennials.

MARTIN H. BENDER [1,2]

JERRY M. BASKIN [1]

CAROL C. BASKIN [1,3]

I. Abstract

A review of age of maturity in herbaceous, polycarpic perennials found that the most common year of earliest maturity for wild and cultivated conditions was the second year of life, followed by the first year and then the third year. A comparison of age of maturity in wild and cultivated conditions for individual taxa confirmed the assumption that perennials generally do not mature sooner in the wild than in cultivation. This validated use of the pattern for maturity in cultivation (second year or later) against which to judge that for maturity in the wild. For plants of the same age of maturity, those with clonal growth had longer life spans than did those with little or no clonal growth. This difference in life span was more pronounced for plants of first- and second-year maturity than it was for those of later maturity. Herbaceous, polycarpic perennials in the wild generally were either short-lived with first-year maturity or long-lived with later maturity. These results were also true for nonclonal taxa only. For application to the real world, theoretical plant-population models must take these results into account.

II. Introduction

Hart (1977) compared the population growth of polycarpic perennials with that of biennials and annuals in a theoretical model. Her results were contradicted by empirical evidence of the prevalence of annuals and biennials in disturbed habitats (Harper, 1977). In our reanalysis of Hart's model, we found that the equation she used for the population growth rate of perennials contained an implicit assumption that long-lived perennials generally matured in the first year of life (Bender & Baskin, 1994). The purpose of the following literature review is to examine the validity of this general assumption for herbaceous perennials. We report the age of maturity and life span for individual taxa and examine the resulting age distributions. We also ascertain the relationship between age of maturity and life span in herbaceous perennials with vegetative reproduction compared with those without it.

In their review of woody and herbaceous perennials, Harper and White (1974) included only four perennials (three herbaceous species and Carica papaya L.) with maturity before the third year of life (i.e., before age 2 on their graph; see below). None of these matured in the first year of life. Hence, we conducted a more comprehensive review to explore the relationship between age of maturity and life span in herbaceous, polycarpic perennials.

III. Methods and Concepts

Data on age of maturity and life span from various studies were arranged into Tables I-VII for taxa in the wild and into Tables VIII and IX for domesticated and wild taxa in cultivation. Each reported value does not necessarily apply in all years or in all the habitats in which the taxon occurs. Authorities for taxa were obtained from Royal Botanic Gardens, Kew (1895-1987), Bailey (1949), Fernald (1950), Munz and Keck (1959), Tutin et al. (1964-1980), and Great Plains Flora Association (1986).

A. AGE OF MATURITY

Age of maturity for each taxon in Tables I-IV and VIII is the earliest one given in a study, even if it was uncommon for individuals to mature that early. Age of maturity for each taxon in Tables V-VII and IX is given as reported in a study, which may include a range or inequality. An inequality without an equal sign (i.e., [greater than] or [less than]) means that the species had not yet matured by the reported age and that its age of maturity thereafter was unknown. Age of maturity in Tables VIII and IX for some perennials in cultivation may be anecdotal.

Age of maturity is for individuals derived from seed, not vegetative means. Individuals derived by vegetative reproduction begin with a larger food supply than do those derived from seed and reach maturity more quickly (Abrahamson, 1980).

B. YEAR OF MATURITY

There is the potentially confusing concept of a plant maturing at age 0 (i.e., during the first year of life). To avoid this problem, maturity was reported as year of life. That is, if a value is reported in a study as age, then one was added to the age to convert it to year of life. Field researchers generally count age incrementally by calendar year, and age does not change within calendar year. Thus, age 0 or year 1 for a plant would be the first full growing season or nearly so (Lacey, 1988). Hence, if a seed germinated in fall, year 1 would be the next calendar year.

C. LIFE SPAN

Although the age of maturity is for genets, in most cases researchers made no distinction between genets and ramets for life span. Harper and White (1974) regarded life span as "normal attainable age," being the age of death for the few individuals that achieve dominance within a population. Life spans were determined by various techniques, such as marking plants or counting annual growth rings. If life span was reported as age, then it was converted to year of life, as above. The largest measured age was 44 years (Schaal & Levin, 1976). Thus, any value 50 years or older was a rough estimate, and the value was left unchanged as it was entered into the tables; that is, one was not added to the age to convert it to year of life.

D. VEGETATIVE REPRODUCTION

Tables I-VI were constructed according to the abundance of ramets relative to that for genets. This is because clonal growth can prolong the life of a genet and thus confound the relationship between life span and age of maturity (Harper, 1977). On the basis of the cited authority, other literature, or personal experience, the abundance of ramets was determined either as common or uncommon (including none) relative to reproduction by seed. As an example, although Allium ursinum (Table V) has ramets known to live longer than two years (Pitelka & Ashmun, 1985), populations studied by Ernst (1979) reproduced much more by seed than by ramets. Thus, we regarded the relative abundance of ramets to be uncommon in this species. Although our assigned relative abundance of ramets could be moot for a few reported species, it should be clear enough for most species so that any general patterns observed in this review are valid. While Table VI contains a few species in the Orchidaceae, Table VII consists of orchids for wh ich the abundance of ramets could not be ascertained by us because little is known about the population biology of orchids.

E. CULTIVATED TAXA

The data for cultivated taxa provide additional evidence that maturity for some perennials in the wild may not occur until the second year or later. That is, if a perennial species required this long to mature under cultivation (Table IX), then the same could be inferred for maturity in the wild, as corroborated by a comparison of age of maturity in wild and cultivated conditions for individual taxa (see Results). It would be unlikely that this species would mature in the first year in the wild, where there are usually less resources per plant than in cultivation.

Age of maturity in the wild could not be inferred for perennials that matured in the first year in cultivation (Table VIII). Even if a species matures within a few months under cultivation, this is no guarantee that it reaches maturity in the first year in the wild. For example, Cryptotaenia canadensis and Talinum calcaricum go from seed to maturity in 10 and 6 weeks, respectively, in the greenhouse (Table VIII), but they do not mature in the first year in the wild (Tables IV and V). Talinum parviflorum, T. calycinum, T. rugospermum, and T. mengesii also mature in 6 weeks in the greenhouse (Table VIII) but are known to grow very slowly in the field (Baskin & Baskin, personal observations).

Age of maturity for 821 cultivated taxa were obtained from reports on genera by Bailey (1914), Hottes (1937), Eliovson (1980), and Schmidt (1980). They listed the perennial species in each genus but gave an age of maturity only for the genus as a whole. Examination of species in genera with multiple reports in Tables VIII and IX shows that species within a genus usually have ages of maturity under cultivation that are not very different. Thus, for a report on a genus, we assumed that all listed species had the given age of maturity. There is some duplication in the species reported by the four authors, but that is small relative to the total of 821 species.

IV. Results

A. YEAR OF MATURITY

Figures 1 and 2 summarize the distribution of the year of earliest maturity in 247 reports for perennials in the wild (Tables I--VI) and 1,432 reports for perennials in cultivation (Tables VIII and IX). The most common year of earliest maturity for wild and cultivated conditions was the second year of life. For wild conditions, this was followed by the first year and then the third year, whereas for cultivated conditions the reverse was true. This would still apply for cultivated taxa if all taxa listed with unknown year of maturity greater than one (shaded bar for cultivated taxa of year 2 in Fig. 2) were eventually found to have year of maturity equal to three. The number of reports in the remaining years of maturity declined monotonically for both wild and cultivated conditions, including individual years greater than ten for wild conditions.

If reports of cultivated genera were excluded from the data set for cultivated taxa, then the second year would still be the most common year of earliest maturity, but followed by the first year and then the third year, the same as the order for wild taxa. The reason for the reversal of the first and third years was that the count for the third year was inflated by large reports of56 species for the genus Lilium and 50 for Gentiana (Table IX). Because of this bias, it would be more valid to conclude for cultivated conditions that first-year maturity was more common than maturity in the third year of life.

B. MATURITY IN THE WILD AND IN CULTIVATION

There were 78 species reported under both wild and cultivated conditions (immediately evident in Tables VIII and IX; cultivated genera were not counted). Comparison of the results showed that although most taxa matured later in the wild than under cultivation, 19 species matured in the same year in both conditions. Ten species did so in the first year of life: Aster pilosus, Plantago lanceolata, P. major, P. rugelii. Rumex crisp us, Anthoxanthum odoratum. Trifolium repens, Kuhnia eupatorioldes, Dalea candida, and D. purpurea (Table VIII). This would be expected because the first seven species are often found in disturbed habitats; the eighth one, usually in dry, sterile soil; and the last two, sometimes on dry, rocky hillsides. Under these conditions, a low level of competition may allow these species to mature as quickly in the wild as under cultivation. Nine species matured in the second year of life in both wild and cultivated conditions: Achillea millefolium, Asciepias syriaca, Tussilago farfara, Rumex c rispus (again), Echinacea tennesseensis, Solidago nemoralis, S. rigida, Arabis perstellata, and Deschampsia caespitosa (Table IX). Again, a low level of competition would allow the first eight species to mature as quickly in the wild as under cultivation because the first four species often are found in disturbed habitats; and the next four, in dry, sterile, or rocky soil. The last species, Deschampsia caespitosa, grows in wet habitats, which would provide resources similar to those in cultivated conditions.

Five of the 78 species matured in the first year of life in the wild but in the second year of life in cultivation: Dalea purpurea, Psoralea tenuiflora, Holcus mollis, Rumex crispus, and Aster pilosus (Table IX). In some cases, this may be due as much to inadequate conditions under cultivation as to benign conditions in the wild, the latter for the following reasons. Dalea purpurea and Psoralea tenuiflora probably encounter little competition, the former in dry, rocky hillside prairies and the latter in overgrazed prairies. Holcus mollis grows in damp places and thus benefits in the same manner as Deschampsia caespitosa. The first-year maturity for Rumex crispus in the wild was for Canadian ecotypes (Table 1), whereas second-year maturity under cultivation was for plants from coastal areas and riverine tidal muds in the British Isles (Table IX). In contrast, inland populations of Rumex crispus from ruderal and arable land matured in the first year of life under cultivation (Table VIII). Aster pilosus grows i n disturbed areas, which provide conditions similar to those of cultivation (Table II). Also, nonserpentine populations of Aster pilosus matured in the second year of cultivation, whereas serpentine populations did so in the first year (Tables VIII and IX).

These results for the 78 species confirm the assumption that perennials generally mature later in the wild than under cultivation because of competition and limited resources. Hence, from the reports in Table IX for maturity under cultivation in the second year or later, it can be inferred that maturity in the wild would usually require just as long a period for the taxa in that table.

C. LIFE SPAN

Results pertaining to the relationship between age of maturity and life span in the wild are presented in Tables I-VII. There were 40 taxa of first-year maturity with reported life span (Tables I and II). Of those, only six had a long life span (verbal description or defined as [greater than] 5 years on the basis of the data in this review). There were 140 taxa of second-year maturity with reported life span or a life span known to be more than 5 years because age of maturity [greater than or equal to]5 years (Tables III-VII). Of these, only five species had a short life span ([less than or equal to]5 years), all in Table III.

Comparison of Table I with Table II, and of Table III with Table IV, shows that among taxa of the same age of maturity, those with clonal growth generally had longer life spans than those with little or no clonal growth. For taxa with reported life spans and first-year maturity, only three of 33 nonclonal taxa had a long life span (Table I), while three of seven clonal taxa were long-lived (Table II). For taxa of second-year maturity, only one often clonal taxa had a life span less than nine years (Table IV), while this was true for 11 of 17 nonclonal taxa (Table III). The difference in life span was not as pronounced between clonal and nonclonal taxa of third-year maturity or later (Tables V and VI).

The confounding effect of clonal growth is removed by comparing only taxa for which ramets are uncommon or absent. Only three of 33 nonclonal taxa with reported life spans and first-year maturity are long-lived (Table I), whereas long life spans are found in nine of 17 and 30 of 30 nonclonal taxa of second-year and later maturity, respectively (Tables III and V). Hence, in the absence of clonal growth, a strong difference in life span remains between taxa of first-year maturity and later maturity.

V. Discussion

The most common year of earliest maturity for both wild and cultivated conditions was the second year of life, followed by the first year and then the third year. The first and third years were common enough relative to the second year that it would be inaccurate to simply approximate the perennial life history as being long-lived and maturing in the second year of life. Instead, the review showed that herbaceous, polycarpic species in the wild generally are either short-lived with earliest maturity in the first year of life or long-lived with later maturity. This also applied to nonclonal taxa only. These observations add more precision to the conclusions for polycarpic perennials made by Harper and White (1974) and supported by those made for trees by Molisch (1938) and Kozlowski (1971): Plants with a brief juvenile period have a short life span, and plants with a long juvenile period have a long life span with a long reproductive life.

Some additional considerations for perennials in wild conditions somewhat offset each other, thus leaving the results for wild taxa roughly the same. First, one could argue that the count for first-year maturity in the wild was inflated by the 19 Senecio species (Table I), which constituted approximately 40% of the wild taxa with first-year maturity. Second, due to constraints by funding and academic policy, research on wild perennials may be biased toward short-lived species and thus toward first-year maturity. Adjustment for these facts could reduce the count for first-year maturity below that for the third year.

However, this reduction in count would be offset by the fact there were many perennials of first-year maturity that we could not report due to lack of information. For example, approximately 60 perennials of first-year maturity were listed by Bennett (1972), Bennett and Smith (1976), and Bennett et al. (1982), but most were without literature citations that would have allowed us to determine whether each species was studied in wild or under cultivated conditions. Moreover, according to the Flora Europaea' (Tutin et al., 1964-1980), some of these species had both annual and perennial life cycles in the wild, so there was uncertainty about life cycle.

A comparison of age of maturity in both wild and cultivated conditions for individual taxa confirmed the assumption that perennials do not mature earlier in the wild than in cultivation. This validates the above use of the pattern in maturity under cultivation (second-year or later) against which to judge that for maturity in the wild.

For plants of the same age of maturity, those with clonal growth had longer life spans than did those with little or no clonal growth. This would be expected, because clonal growth can prolong the life of a genet. This difference in life span was more pronounced for plants of first- and second-year maturity than for those of later maturity. In the latter case, anatomical and physiological mechanisms that keep a nonclonal perennial alive during a long juvenile period also continue on into a long life span approaching that of clonal plants.

In conclusion, the combination of long life span and first-year maturity is not an accurate approximation of perennial life history, as was implicitly assumed by Hart (1977) in her theoretical plant-population model. Such models must take into account that herbaceous, polycarpic perennials in wild conditions generally are either short-lived with earliest maturity in the first year of life or long-lived with later maturity.

(1.) School of Biological Sciences University of Kentucky Lexington, KY 40506-0225, U.S.A.

(2.) Present address: The Land Institute 2440 E. Water Well Road Salina, KS 67401, U.S.A.

(3.) Department of Agronomy University of Kentucky Lexington, KY 40506-0091, U.S.A.

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