a new classification for plant phenology based on flowering patterns in lowland tropical rain forest...

A New Classification for Plant Phenology Based on Flowering Patterns in Lowland TropicalRain Forest Trees at La Selva, Costa RicaAuthor(s): L. E. Newstrom, G. W. Frankie and H. G. BakerReviewed work(s):Source: Biotropica, Vol. 26, No. 2 (Jun., 1994), pp. 141-159Published by: The Association for Tropical Biology and ConservationStable URL: http://www.jstor.org/stable/2388804 .Accessed: 14/09/2012 16:09

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BIOTROPICA 26(2): 141-159 1994

A New Classification for Plant Phenology Based on Flowering Patterns in Lowland Tropical Rain Forest Trees at La Selva, Costa Rica1

L. E. Newstrom and G. W. Frankie

Department of Entomology, University of California, Berkeley, California 94720, U.S.A.

and

H. G. Baker

Department of Integrative Biology, University of California, Berkeley, California 94720, U.S.A.

ABSTRACT A new classification and conceptual framework for plant phenology are proposed to resolve problems in describing tropical patterns. A long-term (12 yr) survey of flowering in 254 lowland tropical rain forest trees of 173 species from the La Selva Biological Station in Costa Rica showed highly diverse, irregular, and complex patterns. Analysis of this survey data relied primarily on graphical analyses that provide data representation methods rather than numerical summaries that provide data reduction methods. The classification differs from previous ones in three ways. It uses, as the primary criterion, frequency of the time series, based on explicit time and amplitude scales, so that irregular temporal sequences are revealed. It features a system of subsidiary classes based on other quantitative descriptors: regularity, duration, amplitude, date, and synchrony. Finally, the conceptual framework separates patterns at each level of analysis so that adding the time series at one level produces a time series for the next higher level. Levels are hierarchical from the flower to the individual, population, and community with additional non-nested levels such as the guild. The four basic classes-continual, subannual, annual, and supra-annual--are applied to patterns at any level of analysis. The classification system provides a logical framework for quantitative description of phenological behavior leading to more standardized comparisons. Thus we can see that tropical phenology differs from temperate phenology in two major ways. In tropical species, the nature of the pattern may change from one level of analysis to the next, which is not typical of temperate species. In many tropical species, phenological patterns vary more widely over the geographic range of a species than they do in temperate species.

Key words: classification; community; flowering; guild; individual; La Selva Biological Station; lowland tropical rain forest; phenology; population; tropical trees.

PLANT PHENOLOGY IS CONCERNED with the timing of recurring events, and in particular is poorly known for lowland tropical rain forest species, although this ecosystem has the greatest diversity of phenological patterns. The paucity of knowledge belies the importance of phenology for understanding the ecology and evolution of species and communities in the tropics. The timing of plant reproductive cycles affects not only plants but also animals that depend on plant resources. It impinges on plant-plant interactions such as competition for resources or for pollinators. The timing of flowering can serve as an isolating mechanism in plant speciation, while the timing of pollinator and disperser activity can limit the range of a plant species. In addition, the timing of seed production can profoundly influence population dynamics.

Plant phenology has been most studied in the

temperate zone. In contrast, tropical phenology has been an imprecise and often confusing discipline, in part because it has been relatively little studied and in part because it has been handicapped by the lack of standardized terms and methods. This paper pro- poses a new classification and conceptual framework that provides a logical system for quantitative description of patterns. A typological approach to phenology not only identifies patterns that may represent adaptive syndromes but also provides a unit of analysis that serves as a context for organizing information. The system can be used for any recurring event in plant or animal life cycles in any region of the world. We have developed it here on the basis of flowering patterns in lowland tropical rain forest trees but any other phenological character can be substituted (e.g., leafing or fruiting).

Most of the phenological work in lowland tropical rain forest has been conducted at the community level to show the overall seasonality of the forest, often with the goal of understanding fruiting cycles

I Received 7 October 1992; revision accepted 4 June 1993.

141

142 Newstrom, Frankie, and Baker

for animals (see references in Newstrom et al. 1993). Very little information exists for long-term individual level patterns because the few long-term surveys that have been conducted have only superficially described individual patterns (Koelmeyer 1959, Medway 1972, Dieterlen 1978, Cruz Alencar 1979).

Our data on long-term (12 yr) leafing, flowering, and fruiting cycles in 254 trees from 173 species in the lowland tropical rain forest at the La Selva Biological Station in Costa Rica have shown four basic patterns at the individual level and gen- erated new insights for the organization of phenological patterns at other levels of analysis such as the population, guild, and community. We focused first on flowering cycles, finding them to be more diverse, irregular, and complex than in any other ecosystem. This presented problems for describing patterns and led to the development of a new classification allowing a more quantitative approach. In this paper, we review the limitations of previous classifications for tropical flowering patterns, then present our classification along with the conceptual framework for using it. We illustrate its utility with examples from individual, population, guild, and community levels of analysis.

PREVIOUS CLASSIFICATIONS Several classifications have been proposed to describe tropical flowering patterns. Classifications that in- corporate additional nonflowering criteria are not discussed here, such as those with leafing (Reich & Borchert 1984) or with life form (Sarmiento & Monasterio 1983). There are three main classifications based on flowering patterns alone. The most widely used classification, based on date or season, has been imported from temperate phenology (Croat 1975, 1978; Tomlinson 1980). Temperate-based concepts, however, frequently break down when applied to characters of tropical plants as has been the case with branching patterns (Tomlinson & Gill 1973) and deciduousness (Richards 1952, Long- man & Jenik 1987). The only classification of flowering phenology devised specifically for the tropics is that of Gentry (1974). This has been the most satisfactory to date of those available and has been used fairly widely (e.g., Morellato and Leitao-Filho 1990, Oliviera et atl. 1991). The striking short- lived displays of flowering in the wet and dry tropics inspired another type of classification based on duration. This has been used in discussions of pollinator foraging behavior and reproductive biology (e.g., Frankie et ail. 1974, Augspurger 1980, Bawa 1983).

CLASSIFICATIONS BASED ON DATE.-Classification systems derived from temperate phenology refer to the date or season of flowering (such as wet, dry, or transition season). Since the categories are usually based on data averaged over a number of years rather than on a time series pattern, the main limitation of this system lies in the implied assumption that the flowering pattern has an annual cycle. Our long-term data show that temporal sequences in the wet tropics are often not annual, although many biologists have a subjective impression that patterns have annual frequency due to annual amplitude peaks. Amplitude is defined as the quantity or intensity of response, for example, the number of flowers on a tree or the number of trees flowering in a population. Categories based on date often do not distinguish annual flowering patterns in an "on"/ "off' cycle from patterns having an annual amplitude peak in a background of lesser flowering all year long. Furthermore, systems based on date of flowering tend to promote a proliferation of terms in the wet tropics where seasons are often not as highly differentiated as they are in the temperate zone. For example, Croat (1978) had 26 categories of flowering for the tropical moist forest on Barro Colorado Island in Panama.

GENTRY'S CLASSIFICATION.-Gentry (1974) created a classification to describe types of flowering for Bignoniaceae in relation to pollination systems. The five major classes, (big bang, multiple bang, cor- nucopia, steady state, and an unnamed pattern), incorporated a mixture of criteria such as individual level amplitude, date, duration, and population level synchrony. Although this system identifies temporal sequences well, it does not encompass the range of diversity found in our data. The classes have been used imprecisely in the literature because some authors have used them for patterns that do not meet all of the criteria originally specified by Gentry. Furthermore, the original definitions of some patterns include both individual and population level criteria but phenologists have frequently not specified these levels of analysis and often have data from only one level but not both.

CLASSIFICATIONS BASED ON DURATION.-Systems based on duration distinguish between extremes of short and long duration of flowering, e.g., "seasonal" vs. "extended" (Frankie et al. 1974), "mass" vs. "steady state" (Augspurger 1983), and "mass" vs. "extended" (Bawa 1983). As with categories based on date, such classes do not reveal the temporal sequence and lack explicit time and amplitude scales.

Plant Phenology 143

A major problem with this system is that some terms refer to many different types of patterns. For example, "mass" has been used not only for flowering that lasts for a few days or weeks (Augspurger 1980, Appanah & Chan 1981), but also for many weeks or months (Perry & Starrett 1980, Appanah 1982). It has referred to patterns at a number of different frequencies (from several times a year to multiyear cycles) and to many different levels of analysis (such as individual, population, and community). For example, "mass" (and related terms such as "general" and "gregarious" flowering) has referred to high amplitude flowering with multiyear cycles that are synchronized among many species at the community level (Janzen 1978, Silvertown 1980, Ashton 1988).

PROBLEMS IN TROPICAL PHENOLOGY PATrERNS THAT ARE NOT REVEALED.-Because cycles are so complex and irregular, the main problem in tropical phenology is pattern recognition. Thus the role of graphics and choice of graphical style has critical importance. Numerical summaries have often obscured temporal sequences in tropical phenology (e.g., reports of 5 mo reproductive cycles in figs (Koelmeyer 1959) and 7 to 10 mo cycles in Delonix regia and Lagerstroemia speciosa (Richards 1952) lack a measure of variance and therefore do not readily reveal irregularity in cycle lengths). Ex- ploratory Data Analysis (Tukey 1977) and the in- creasing power of computers and software have spawned the field of graphical analysis (Cleveland 1985). Graphics can reveal unexpected relationships because they display large amounts of information while retaining the relative arrangement of points in a way that numerical summaries cannot (Tufte 1983, Cleveland 1985, Pickover 1990). By using graphs rather than numerical summaries in phenology, formerly obscure flowering patterns can be revealed (see below). Our search for new phenological patterns has been expedited by rapid gen- eration of thousands of computer graphs, an im- possible task by hand.

The choice of graphical style may obstruct or aid pattern recognition. In tropical phenology, tra- ditional graphs have served as visual obstacle courses more than as tools for pattern recognition whenever- they superimpose multiple events (e.g., leafing, flowering, and fruiting) along the same time axis using either line plots or a variety of different symbols (e.g., Medway 1972). To perceive the meaning

of these graphs, the reader must not only extract the nature of a given pattern from a complicated overlay of several patterns, but also spend consid- erable time and memory encoding and decoding numerous symbols. Cleveland (1985, p. 25) re- solved this problem for other types of data by jux- taposing the events along the same time axis using the same symbols. Following these and other principles of graphics in Cleveland (1985), we have developed new types of graphical displays to produce greater visual clarity for tropical phenology patterns.

PATTERNS THAT ARE NOT COMPARABLE-One of the main problems impeding a synthetic treatment of tropical phenology has been difficulty in comparing results among studies due to a lack of standardization in terms and methods (Frankie et al. 1974, Bawa & Hadley 1990). There are several reasons why tropical phenology terms are often ambiguous. In many cases, the same term has been used for several different phenomena (such as "mass" or "steady state"), or the same phenomenon has been measured with many different methods, or different time or amplitude scales. Conversely, a profusion of different terms may refer to the same pattern. For instance, subannual flowering in our classification has been refered to as "episodic" (Bullock et al. 1983), "periodic" (Haber & Frankie 1989), "intermittent" (Koelmeyer 1959, Medway 1972, Berg 1989) and "multiple bang" (Gentry 1974). In our classification, we have therefore used consistent and precisely defined criteria, incorporated explicit time and amplitude scales, and restricted the number of terms employed (see glossary in Appen- dix and discussion in Newstrom et al. 1993).

PATTERNS THAT ARE CONFUSED AT DIFFERENT LEV-

ELS.-Part of the complexity of tropical phenology is due to the differences in patterns from one level of analysis to another (see Table 1). Although several authors distinguished between individual and population levels (e.g., Augspurger 1980, 1981; Piiiero and Sarukhan 1982; Bullock et al. 1983), phenologists have not systematically incorporated levels of analysis into the language of tropical phenology. This is due to the common assumption that patterns are the same at all levels for a given species, which is often true for temperate phenology where winter synchronizes most species into annual cycles at all levels. However, it is not true for tropical phenology where patterns may differ at different levels of analysis as illustrated in the examples below.


METHODS Data collection procedures for this project and site information for the La Selva Biological Station in Costa Rica have been described in Frankie et ail. (1974) and Newstrom et ail. (1993). Using bin- oculars, monitors made monthly observations of leafing, budding, flowering, and fruiting on 457 tagged trees from January 1969 to March 1981. Only those trees with a minimum of 5 consecutive years of observations were used for the classification, resulting in a sample of 254 trees representing 173 species in 59 families. In this sample, 11 species were represented by 4 to 6 trees, 78 species by 2 or 3 trees and the remainder by one tree. The amplitude scale had three classes: none, light, and heavy flowering with respect to the typical crop of flowers for each tree. Wherever there were three or four trees available for a given species in our data, we estimated a population level pattern by calculating the proportion of trees in flower at each interval in the time series. Seasons at La Selva have been clas- sified as main dry from January to May; early wet from May to September; veranillo, an unpredictable dry season, in September or October; and, late wet from October to January (Newstrom et ail. 1993).

BASIC CLASSIFICATION.-The patterns form a continuum from continuous to very infrequent flowering. We distinguished four basic classes based on frequency, defined as the number of "on'" /"off" cycles per year (one cycle consists of a flowering episode followed by a nonflowering interval, Fig. 1). The four basic classes are continual (flowering with sporadic brief breaks), subannual (flowering in more than one cycle per year), annual (only one major cycle per year), and supra-annual (one cycle over more than one year) (Figs. 1 and 2). Regularity, used in the classification as a secondary criterion, is defined as the variance in length of flowering episodes and nonflowering intervals, and consequently of the cycles as well (Fig. 1). We initially recognized two main classes, regular and irregular, but are presently quantifying this criterion in more detail.

The classification uses other criteria such as duration, amplitude, and date to further subdivide the classes (see Newstrom et al. 1993). For example, we divide annual flowering patterns into three durations: brief flowering (< 1 mo), intermediate flowering (1-5 mo), and extended flowering (>5 mo). We base other subcategories on the shape of the curve for amplitude of flowering (see Fig. 11.8 in Newstrom et ail. 1993). Further subdivisions are based on date, represented as the month or season.

00

00

00

ON 00 ON ON ON

0 -., -4 4.4 60 , , oo tc C) .- 00 0 00 00 " ON 0

CZ 00 00 r- r- 0 CZ Z

44 z ON 0 CZ -a

-4 4

tu

Z 44

x ol CZ

0 0

7:1

-0 C:

Plant Phenology 145

Continual FREQUENCY CLASSES 24

12 24 36 48 60 72 84 96 108 120 132

12 24 36 48 60 72 84 96 108 120 132

Sub-annual 24-

04.

*3 ']. 11; 11, ---. ---,-- * ,;11 1 I 1 1; 1;. 1,

12 24 36 48 60 72 84 96 108 120 132

Annual

0 .. . . . . . . .. . 0 .... .. . .. ; . . . . . . .. . ... . . . I....... .. . I. . . . . I. . . . . ... . . . I. .. ...... . 1 1.. ; .. .. ?

12 24 36 48 60 72 84 96 108 120 132

0

2S~upra-annual

01

12 24 36 48 60 72 84 96 108 120 132

REGULARITY CLASSES Regular pattern 21

12 24 36 48 60 72 84 96 108 120 132

Irregular pattern 21 o .. .. . . .. .. .. . ; .. . . . .;.. . . . . .. .. .. .. . . . . . . . .. . .. . .

12 24 36 48 60 72 84 96 108 120 132

Time: 144 months FIGURE 1. Idealized diagram of four frequency classes and two regularity classes with amplitude held constant to reveal the essence of each criterion.


We reserve the term seasonality to mean the temporal association of flowering with a certain month or season of the year and not to refer to an annual frequency as is commonly done in phenology literature. Thus, any of the four basic frequency patterns can have seasonal associations related to the dates when flowering most often occurs or when flowering is heaviest.

THE INDIVIDUAL LEVEL.-Three different graphical presentations characterize the four basic patterns: time series graphs (high density plots in S program, Becker et al. 1988) show the frequency and regularity of cycles (Fig. 2), matrix graphs show the duration and date (Fig. 3, lower half), and bar graphs portray seasonality of flowering frequency and amplitude (Fig. 3, upper half).

In the continual pattern, shown in Guatteria aeruginosa (Annonaceae), flower production ceases

only sporadically and briefly (Figs. 2 and 3). Con- tinual patterns have seasonal trends for higher prob- ability of heavy flowering (e.g., in both dry seasons in Guatteria aeruginosa (Fig. 3, upper half) and both wet seasons in Hamelia patens (see Fig. 11.7 in Newstrom et al. 1993)).

The subannual flowering pattern is the most irregular and poorly understood. The pattern, as shown in Protium pittieri (Burseraceae), has several unpredictable flowering cycles per year (Figs. 2 and 3). Although a few years have only one cycle of flowering, most years have several. This illustrates the importance of long time series (at least 5 yr) to fully describe patterns in tropical phenology, although some patterns may be inferred from short term population studies. Three distinctive features characterize this pattern: flowering episodes occur at any time of the year, both flowering episodes and nonflowering intervals vary greatly in duration, and

Continual Guatteria aeruginosa Tree 1043

1-lll llll l l Hl iii Hl iii ll lt lll iii iii ii ll iii 11111 iil ill ilt,lll ii I , 12 24 36 48 60 72 84 96 108 120 132

a)

Sub-annual Protium pittieri Tree 1102

r_: 2 -~

~~~~~~~8 60 7 4 6 18 2 3

o0 2 0 , .. ..... .......... 1 ... t ....... IlI.,II - .1 1111!l .11 11 .,.... 1.1 l!ll l11 1II 1II ! 11 .

E Annual ~Lonchocarpus oliganthus Tree 1004

j I2 I I I, I. 11111 1 12 24 36 48 60 72 84 96 108 120 132

Supra-annual Sapranthus campechianus Tree 2173 2 -

I . .. . .... . I........ ...... I .......1..1.. .. ...... . - - - . - .1 12 24 36 48 60 72 84 96 108 120 132

Time in months: Jan 1969 - Dec 1980 FIGURE 2. Time series graphs showing the frequency and regularity in four basic flowering patterns (S program high density plot in Becker et al. 1988). Each graph shows monthly flowering from 1969 to 1980 for one tree of each of four species in the lowland tropical rain forest at the La Selva Biological Station. Amplitude categories are: I = light flowering, 2 = heavy flowering, dots on the x axis = no flowering, blanks = missing data.

Plant Phenology 147

consequently the number of cycles per year varies as well. These patterns have seasonal associations for both when flowering occurs most often and when flowering is heaviest. In the case of P. pittieri, most flowering occurs in the early wet season at La Selva but in other species, such as Guarea rhopalocarpa (Meliaceae) and Compsoneura sprucei (Myristicaceae) most flowering occurs in both dry seasons (see Fig. 11.7 in Newstrom et al. 1993).

Annual flowering has only one major flowering episode per year, as illustrated in Lonchocarpus oliganthus (Fabaceae) (Figs. 2 and 3). This pattern is the most regular one and has the most consistent durations for both the flowering episodes and the nonflowering intervals. This pattern usually has major flowering episodes that are constrained to one

time of the year. Variations of the annual pattern include the pulsed annual pattern with pauses em- bedded in the major flowering episode as found in Vellozia squamata (Velloziaceae) in the cerrado of neotropical Brazil (Oliveira et al. 1991) and in Melicytus ramiflorus (Violaceae) in temperate New Zealand (Powlesland et al. 1985); and patterns with additional low amplitude precocious or tardy brief bursts of flowering that sporadically occur outside the main flowering episode (see Fig. 11.8 in News- trom et al. 1993).

Supra-annual flowering, shown in Sapranthus campechianus (Annonaceae) has flowering episodes in multiyear cycles (Figs. 2 and 3). Some supra- annual patterns have rare flowering (one or two in 12 yrs) but others have approximately "alternate"

CONTINUAL SUB-ANNUAL ANNUAL SUPRA-ANNUAL Guatteria Protium Lonchocarpus Sapranthus aeruginosa pittieri oliganthus campechianus Tree 1043 Tree 1102 Tree 1004 Tree 2173

CIO

1.0

0.5 '11i111 111111.I. 0.0-

JFMAMJJASOND JFMAMJ JASOND JFMAMJ JASOND JFMAMJ JASOND

69 .00. 00 70 .0000000000.so**.*..... 71 * 000 0. 72 - **0 0.0 73 ----00- 74 000@

t8 75 ---- @ 00 0 000000 >-4 76 00.- 00.000 @0 0

77 @000O000 @0 0 78 000 0000 @0 79 *0* . @0000 80 @ 0

81 @001 l l

JFMAMJJASOND JFMAMJJASOND JFMAMJJASOND JFMAMJJASOND

Month FIGURE 3. (a) Upper panel: Bar graphs showing seasonality in four basic flowering patterns as proportion of years in which heavy or light flowering occurred for each month of the year. Each graph shows flowering for one tree from 1969 to 1980 from each of four species in the lowland tropical rain forest at the La Selva Biological Station. Light shading = light flowering, dark shading = heavy flowering. (b) Lower panel: Matrix graphs (yr by mo) showing duration and date in four basic flowering patterns. Each graph shows one tree for the same species as the seasonality bargraphs above. Dark shaded circles = heavy flowering, light shaded circles = light flowering, blanks = no flowering, dots = missing data.


flowering every two to several years These patterns have too few data to determine the regularity, duration, or seasonality of flowering and will not be discussed further in this paper (see discussion in Newstrom et al. 1993).

THE CONCEPTUAL FRAMEWORK We separated patterns at each level of analysis so that adding the time series at each time interval at one level produces a time series pattern for the next higher level (Table 1, Figs. 4 to 6). Levels are hierarchically arranged: flower, inflorescence, branch, branch complexes, individual, population and community with additional non-nested levels such as the guild. The four basic frequency classes are ap-

plied to any level of analysis. Profiles of the relative abundance of patterns comprising each level demonstrate the diversity of patterns in tropical phenology (see community histogram below). Unlike temperate species, tropical species commonly have heterogeneous patterns at a given level. For example, a population may be composed of individual patterns that differ because of age and size (Borchert 1978), gender (see Fig. 6 for Compsoneura sprucei and Fig. 11.6 in Newstrom et al. 1993), or mi- crohabitat differences. In addition, patterns can differ from one level of analysis to the next, especially in tropical phenology (Table 1).

THE POPULATION LEVEL.-At the population level, the flowering pattern may be simple and composed of only one type of individual pattern, or mixed

Lonchocarpus oliganthus

Annual Tree 1003

12 24 36 48 60 72 84 96 108 120 132 144

Annual Tree 1004 2~ 2

S 12 24 36 48 60 72 84 96 108 120 132 144

Annual Tree 1196

3 .......... 1 .......I .. .. . 1 1 . . 11 11 1 . . . . . . .

12 24 36 48 60 72 84 96 108 120 132 144

Proportion of all three trees in flower

1.0 1 ll l 0- ......

1 I III . 0 .

I . . . . . . . . . . . . . . . . . . . . .

I . . . . . . . . .

I . . . . . . . . . . . . . .

12 24 36 48 60 72 84 96 108 120 132 144

Time in months: Jan 1969 - Mar 1981

FIGURE 4. Estimate of possible annual pattern at the population level based on three annual flowering patterns in individual Lonchocarpus oliganthus trees. The top three panels each represent a time series for one tree. The bottom panel represents the sum of the three individual patterns calculated as the proportion of trees flowering in each month of each year. More than three trees are needed for a better estimate of population patterns.

Plant Phenology 149

and composed of more than one type. The organization of individual level patterns into population level patterns is straightforward for continual and annual flowering but not for subannual (Table 1). A population containing a continual individual pattern always has a continual population pattern. Sim- ilarly, a population with only annual individual patterns always has (as far as we know) an annual population pattern as in Dipteryx panamensis (Perry & Starrett 1980, Newstrom et al. 1993) and pos- sibly in Lonchocarpus oliganthus (as suggested by the three trees in our data in Fig. 4).

In a population with only subannual individual patterns, however, the population pattern will be either continual or subannual depending on the number of trees and the degree of synchrony among trees. Subannually flowering individuals of Guarea

rhopalocarpa (Fig. 5), a dioecious understory tree at La Selva, appear to have sufficient population level synchrony to produce a subannual population pattern with 119 trees (Bullock et al. 1983). The synchrony, in this case, occurs more in the nonflowering intervals than in the flowering episodes, sug- gesting that conditions inhibiting flowering may govern the pattern (see Newstrom et al. 1993 for further discussion). In contrast, more asynchronous populations would produce a more nearly continual pattern, such as we have estimated from four trees of Compsoneura sprucei, an understory dioecious tree at La Selva (Fig. 6). In this species, two types of individual patterns, subannual and annual, appear to be correlated with gender (see Bullock 1982 and Newstrom et al. 1993), although more data are needed to confirm this. The gender difference fol-

Guarea rhopalocarpa

Sub - annual Male tree 1020

ot . 11.111 1III. .1,11 ll I ., I l . ,11 1,1 1 1 ,1 1

1I I 12 24 36 48 60 72 84 96 108 120 132 144

Sub - annual Female tree 1048

t: oq I 111111 1 11l 11 11lll 11 11ll 1111,1, 1~ ~~~~~~~1 11 1.111 .;_ d~~~~~~~~~~~~~~ 12 24 36 48 60 72 84 96 108 120 132 144

Sub - annual Female tree 1149

0 .H..... .......... ... .. . . ... ...... .. 12 24 36 48 60 72 84 96 108 120 132 144

Proportion of all three trees in flower 1.0 -f

os~~~~~~~~~ | || | | 1|||11 11 1 11 1110ll1l.I1 1111

12 24 36 48 60 72 84 96 108 120 132 144

Time in months: Jan 1969 - Mar 1981 FIGURE 5. Estimate of possible subannual flowering pattern at the population level based on four sub-annual flowering patterns in individual Guarea rhopalocarpa trees. Arrangement of graph same as in Figure 4. The subannual population pattern for this species at La Selva is confirmed by data from 119 trees in Bullock et al. (1983).


lows the trend shown in many other species with male plants flowering more frequently than females (Lloyd & Webb 1977, Bawa 1983, Clark & Clark 1987). Selection for subannually flowering trees to form a strictly continuous population pattern occurs in figs, where local survival of fig-wasp pollinators depends on the constant availability of reproductive trees (Newstrom et al. 1993). A reinterpretation of fig phenology using our classification is being presented elsewhere.

THE GUILD LEVEL.-Guild level patterns have four important characteristics. The presence of gaps (or nonflowering intervals) in the multispecies sequence affects the maintenance of the pollinator population throughout the year. Continual guild patterns have no gaps and annual guild patterns have significant gaps during which pollinators are dormant or ab- sent. The amount of overlap among species affects the degree of interspecific pollen mixing and may be related to competition for pollinators (Rathcke

Compsoneura sprucei

Sub - annual Male tree 1009 2-

12 24 36 48 60 72 84 96 108 120 132 144

Sub - annual Male tree 1141 2-

1 i I 1 1, I I .1 111 I. I .......... 1 .. 1 1.... ....1 IJ I11 11l . .. . . I ... I . . . .. 1 .. ..I.. 1 . I 1 11 1 .1 l 12 24 36 48 60 72 84 96 108 120 132 144

Sub- annual Female tree 1118 21-

,C HI 11111 I I I I IIII 11, 11 1I I! 1III H0- 11.11.1l .4 0

12 24 36 48 60 72 84 96 108 120 132 144

0

Annual Female tree 2054

o . . . . . . . . . . . . I . . . . . . I . ... . . . . . . I . . I . . . . . . . . . . . . . . . . I . . . . . . I . . . . . . .

12 24 36 48 60 72 84 96 108 120 132 144

Proportion of all four trees in flower 1.0 -

3.5

12 24 36 48 60 72 84 96 108 120 132 144

Time in months: Jan 1969 - Mar 1981

FIGURE 6. Estimate of a possible population pattern approaching a continual pattern based on three subannual and one annual flowering patterns in individual Cornpsoneura sprucei trees. Arrangement of graph same as in Figure 4. More than four trees are needed for a good estimate of this population pattern. There appears to be a trend for males to have subannual individual patterns and females to have annual individual patterns, but confirmation of this requires a larger sample of trees than in our data and a longer time series than in Bullock (1982).

Plant Phenology 151

1983, Rathcke & Lacey 1985, Pleasants 1990, Newstrom et al. 1993). Changes in amplitude of flowering affect the numbers and level of activity of the pollinators (Bawa 1983, Rathcke & Lacey 1985). Finally, the permutations of the species may be retained in the same order from year to year if each species is strongly and differentially cued, as is common in environments with marked regular seasons. We have identified five types of pollinator guild patterns using our classification (Table 1).

The staggered annual flowering pattern at the guild level is one of the most familiar because it is so common in the temperate zone. In the tropics, it occurs in both wet and dry forests. The pattern comprises a progression of annual population patterns in a sequence of species that extends for only part of the year. For example, in lowland tropical rain forest at La Selva beetle pollinated species flower in a staggered sequence for part of the year (Young 1986, 1990). During the nonflowering interval or gap the beetles are dormant. In the tropical dry forest in Guanacaste, Centris and other large bee pollinated species flower in a staggered sequence during the dry season when a profusion of flowering occurs on leafless trees (Frankie et al. 1976, 1983). The bees are in diapause during the gap in the wet season. Whether or not these patterns have significant overlap has not been statistically tested. The permutations of species are similar each year.

The staggered continual flowering pattern at the guild level occurs in hermit hummingbird pollinated species at La Selva (Stiles 1978). This pattern comprises a yearlong continual sequence of 10 different species with annual population patterns (Fig. 7). Only one minor gap occurred in 1973 in this example when Costus ruber (species 5) did not flower. These species did not overlap significantly (Stiles 1979, 1985; Cole 1981; Pleasants 1990 and see discussion in Newstrom et al. 1993). Yearly bi- modal peaks in amplitude of flowering (Fig. 7, lower panel) are correlated with hermit hummingbird breeding and moulting times (Stiles 1975, 1977, 1978, 1980, 1985). The order of permutations of species was similar each year with only minor variations (Fig. 7).

The mixed continual flowering pattern at the guild level with annual cycles of amplitude peaks contrasts with the staggered continual pattern main- ly because of the extensive overlap and the disor- dered permutation of species each year. For example, 27 species of plants pollinated by nonhermit hummingbirds at La Selva (Stiles 1978), consist of overlapping populations with many different flowering patterns including continual, subannual, and

annual (Fig. 8). This mixed sequence had no gaps, extensive overlap, and a strong unimodal seasonal peak. This example was illustrated by Stiles (1978) as an average for the four years rather than a time series, but presumably the order of species flowering each year changes because of the inherent irregularity of subannual patterns. The mixed pattern has not been well-studied but it probably dominates in pollinator guilds of lowland tropical rain forest because of the prevalence of subannual flowering patterns (Newstrom et al. 1993). The staggered sequence may dominate in more seasonal ecosystems such as temperate and tropical dry forests. The effects of an overlapping mixed multispecies sequence with unpredictable species permutations on pollinator spe- cialization and foraging patterns have not been investigated.

Some mixed continual flowering patterns at the guild level have dramatic amplitude peaks at supra- annual frequencies. This guild pattern has been described for thrip pollinated species in Malaysia (Chan & Appanah 1980; Appanah & Chan 1981; Ap- panah 1985, 1990; Yap & Chan 1990; La Frankie & Chan 1991). After many years of sporadic light flowering, a staggered but slightly overlapping sequence (Ashton et al. 1988) of six Shorea species burst into full, high intensity flowering. At this time, the short-lived thrip pollinators have an exponential population explosion. At other times, other species that flower more frequently at low or intermediate amplitudes maintain the thrips at low population levels.

A specialized continual flowering pattern at the guild level in fig species comprises both subannual and supra-annual individual patterns at the individual level (Milton et al. 1982, Michaloud 1988, Windsor et al. 1989). In this case the guild level is equivalent to the population level because the pollination system is species specific. The continual pattern at the guild level is essential for fig-wasp survival and the subannual pattern at the individual level may be selected because it enhances the pollinator attractant and promotes outcrossing (Janzen 1979, Bronstein 1989, Frank 1989, Bronstein et al. 1990, Newstrom et al. 1993).

THE COMMUNITY LEVEL.-Although the community level pattern has been examined for a number of lowland tropical rain forests (e.g., Koelmeyer 1959, Medway 1972, Dieterlen 1978, Cruz Alencar et al. 1979, Putz 1979, Van Schaik 1986) the range of diversity in population and individual patterns has not been well described. The profile of individual patterns, calculated as the relative abundance of each


type of flowering pattern for La Selva, shows that more trees had subannual (55%) and annual (29%) flowering patterns than continual (7%) and supra- annual (9%) ones (Fig. 9). Within the tree community at La Selva, canopy and subcanopy strata have different profiles (Newstrom et al. 1991). Different types of tropical rain forests may have different profiles in relation to changes in rainfall

distribution or floristic composition. For example, supra-annual flowering patterns may dominate in dipterocarp forests of Malaysia. Major ecosystems show large differences in phenological profiles. For instance, temperate forests have annual community patterns with species having two main population patterns (annual and supra-annual) in contrast to lowland tropical rain forests that have continual

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Plant Phenology 153

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community patterns with species representing all four types of population patterns.

GEOGRAPHIC VARIATION IN PHENOLOGICAL PATrERNS.-Tropical species often have flowering patterns that differ dramatically in different ecosystems, consequently we cannot always describe a tropical species as having a "typical" flowering pattern (Borchert 1980, 1986; Huxley 1983; Akunda & Huxley 1990). The geographic variation in phenological patterns within the same species is more noticeable in the tropics than the temperate zone because phenological diversity is higher. In some species, the flowering patterns are invariant over a wide range of environmental conditions. For example, Cedrela odorata, Cordia alliodora, and Cas- tilla elastica all have the same annual seasonal cycle in the lowland tropical rain forest at La Selva (Fran- kie et al. 1974), the tropical moist forest at Barro Colorado Island in Panama (Croat 1978), and the tropical dry forest at Guanacaste in Costa Rica (Frankie et al. 1974). Possible environmental in- fluences on flowering that are in common in these different ecosystems have not been explored for these species.

In other species, patterns change dramatically from one ecosystem to another. Some species change to a higher frequency of flowering in the wet tropics than in the dry tropics. For example, in the lowland tropical rain forest, trees of Hamelia patens flower

FIGURE 8. Mixed continual flowering pattern at the guild level in nonhermit hummingbird food plants averaged over 4 yrs from 1971 to 1975 in the lowland tropical rain forest at the La Selva Biological Station. The guild pattern comprises continual flowering in species number 1 and 2, subannual flowering in species number 3 to 6, and annual flowering in species number 7 to 27. The populations of 27 species flowered with no gaps and extensive overlap. The permutations presumably change each year because of the unpredictable flowering time in subannual patterns. Species are: I = Cephaelis tomentosa, 2 = Hamelia patens, 3 = Symzphonia glohulifera, 4 = Colurmnea nicaraguensis, 5 = Colusmnea linearis, 6 = Vrie- sea gladioliflora, 7 = Aechmea mexicana, 8 = S-hlegelia sp., 9 = Aechmea maria-reginae. 10 = Gesneriac-eae sp., 11 = Gurania levyana, 12 = Gurania c-ostaricensis, 13 = Odontonema tubiforme, 14 = Aechmea nudi-aulis, 15 = Renealmia exalta, 16 = Heliconia mariae, 17 = Erythrina cochleata, 18 = Cephaelis elata, 19 = Heliconia latispatha. 20 = Besleria sp., 21 = Renealmia cernua, 22 = Guzm,ania monostachia, 23 = Warscewiczia coccinea, 24 = Heli-onia imbricata, 25 = Heliconia sarapiquensis, 26 = Alloplectus coriaceus, 27 = Razisea spicata. (Adapted from Figure 4 in Stiles 1978.)


in a continual pattern with lightest flowering in the dry seasons, while in the tropical dry forest, trees of this species flower in an annual pattern with no flowering in the dry season (Frankie et al. 1974). This pattern shift suggests that lack of moisture inhibits flowering in this species. The influence of hydroperiodicity on flowering patterns has been investigated in many tropical dry forest species (Borch- ert 1980, 1983, 1991; Reich & Borchert 1982, 1984) but has not been studied in lowland tropical rain forest species.

The reverse pattern shift occurs in other species. These change to a lower frequency of flowering in the wet tropics than in the dry tropics. For example, in both Andira inermis and Ceiba pentandra trees flower less frequently, in rare supra-annual patterns, inside the lowland tropical rain forest and more frequently, in alternate supra-annual patterns, in the tropical dry forest and along edges of the lowland tropical rain forest (see Newstrom et al. 1993). In Africa, C. pentandra flowered regularly in an annual pattern in the dry forest and in a supra-annual pattern in the wet forest (Baker 1965). Shorea species in Malaysia demonstrate a similar pattern with trees flowering most often and regularly in drier forests, supra-annually in wet forests, and hardly at all in swamp forests (Yap & Chan 1990). This suggests two possible mechanisms: a dry period may be required for floral bud induction ("xeroinduction, Bernier et al. 1981) or higher light conditions may promote greater flowering frequency. Experi- mental evidence for "xeroinduction' of flowers in the lowland tropical rain forest exists for the her- baceous Geophila renaris (Bronchart 1963, Bernier et al. 1981) but this has not been investigated for trees.

A change from irregular subannual flowering pattern to two regular crops per year with intro- duction of drought has been reported for Citrus trees (Monselise & Goldschmidt 1982) but, oth- erwise, reports of changes involving subannual flowering are rare because this pattern has not previously been well recognized.

CONCLUSIONS The effectiveness of a classification scheme depends on several factors: the importance of the criteria that are given priority for delineating categories, the degree of similarity among members in each category, and the degree of difference among categories (i.e., frequency of intermediates). The more consistent the associations among descriptors for categories, the more successful the classification. If the char-

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FIGURE 9. Histogram of relative abundance of individual patterns making Lp the continuLal flowering pattern at the tree community level in the lowland tropical rain forest at La Selva Biological Station. The four basic patterns are represented as percentages of individuLal trees. This is the appropriate uinit of analysis. The same data calculated as percentage of species rather than trees give similar results. Only trees with - 5 yr of consecutive data were included, and intermediate flowering patterns and palms were excluded.

acteristics are distributed randomly among classes or if classes intergrade in a continuum, the classification has less usefulness. The most important stricture about classifications, however, is that they do not become so rigidly used that they limit creative perception whenever new contexts are more appropriate (Bohm & Peat 1987). We therefore present this classification as a convenient way to bring order to the complexity of phenological patterns in the wet tropics and not as a replacement for previous classifications.

The main contribution of this classification has been to clarify the differences in tropical patterns at different levels of analysis and to provide a logical system for quantification. The results of our quantitative description for patterns using the variables of frequency, regularity, duration, amplitude, date, and synchrony, will be published elsewhere. Using frequency of "on"/'off" cycles based on an annual time scale as the criterion for dividing the classes rather than yearly seasonal averages portrays temporal sequences more clearly, particularly for irregular subannual and supra-annual patterns. The explicit time and amplitude scales permit standardized comparisons among studies. For example, differ-

Plant Phenology 155

entiating "on''/off' cycles from other cycles defined according to amplitude peaks would clarify descriptions of phenological patterns such as the annual patterns reported in fig species by Frank (1989). In our classification, this fig pattern is described as subannual individual patterns which com- bine to form a continual population pattern having strong annual amplitude peaks. The simplicity of using the same four basic patterns at each level of analysis reduces the complexity of tropical flowering patterns and eliminates a confusing proliferation of terms.

Each of the levels of organization has its own value for description of phenology. The individual level is the central one, corresponding to the obvious functional and genetical entities in a population. At the individual level, long time series from tagged trees furnish information for studying physiological mechanisms such as response to environmental cues or endogenous rhythms in the context of differences in age, size, genetical composition, gender, or mi- crohabitat. The subindividual levels, flower, inflorescences, and branch allow the behavior of individuals to be analyzed more closely. At the population level, interpretations can be made for pollination and dispersal systems, as well as aspects of demography and reproductive biology such as plant mating systems and gene flow. At the guild level, the group of plant species shared by one group of animals such as pollinators or frugivores shows how broader ecological and evolutionary factors have led to the organization of plant-animal interactions. At the community level, questions of community ecology, biogeography, and floristics can be ad- dressed.

In summary, we propose a new classification for phenological patterns to resolve several problems

in describing flowering phenology in lowland tropical rain forest trees. The classification captures the full range of diversity and clearly reveals irregular temporal sequences that are so common in this ecosystem. Four basic patterns (continual, subannual, annual and supra-annual) are applied to descriptions of patterns at each level of analysis from the flower to the individual, population, or community as well as the guild. The quantification of patterns promotes standardization, one of the major problems in tropical phenology. This system sim- plifies the complexity and accentuates the diversity of tropical flowering patterns, and thereby opens the way to more meaningful and accurate comparisons among phenological studies. The scheme has wide application not only for other characters of plant phenology, such as leafing and fruiting, but also for animal phenology as well. It should now be possible to address temporal questions about the ecology and evolution of tropical plant-animal interactions with more precision.

ACKNOWLEDGMENTS

We thank D. G. Lloyd and L. McDade for reviewing this manuscript. For helpful criticism of earlier versions of this classification we are grateful to K. S. Bawa, R. Borchert, R. Colwell, E. 0. Guerrant, P. Hall, S. Koptur, S. Naeem, G. Orians, J. Rosenthal, and F. G. Stiles. We thank J. Frankie, R. Echeveria, C. Esquivel, G. Hart- shorn, and F. G. Stiles for assistance in recording observations, monitoring collection of data, and verifying species names. OTS and NSF funded data collection. Funding for data entry and analyses was provided by OTS, NSF, and the Department of Entomology at the University of California, Berkeley. J. Barthell assisted with data entry and verification. G. Casterline, S. Jacobson, T. Porco, and P. Spector kindly provided consultation for statistical and graphical methods.

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APPENDIX: TERMINOLOGY

Tropical phenology lacks precisely defined and consistently used terms for describing patterns. Quantitative descriptions of the patterns using the variables of frequency, regularity, duration, amplitude, date, and synchrony will be published elsewhere. As these variables are not necessarily independent, we are conducting a study of their inter-relationship. To avoid proliferation of new terms we use the same terms for any phenological event (leafing, flowering, and fruiting) and for patterns at all levels of analysis; therefore, leafing and fruiting can be substituted for flowering in the following definitions. We have avoided using terms that introduce confusion with literature from other fields such as tree development, chronobiology, and the description of oscillations in physics. For this reason, the terms period, periodic and phase are not used here. We prefer to retain their mathematical definitions as used in time series analysis. The definitions of flowering episode and nonflowering interval replace the definitions of flowering and nonflowering phase given in Newstrom et al. (1993).

Amplitude is the quantity of activity, or intensity of response, such as number of flowers on a tree, or flowering trees in a population, or species in a guild or community. A flowering episode may have multiple flowering amplitude peaks which can be measured or estimated qualitatively or quantitatively (e.g., Frankie et al. 1974, Opler et al. 1980, Augspurger 1983). Counting number of inflorescences, however, may be practical only in understory plants (e.g., Bullock et al. 1983). The problem of resolution arises here as broader categories obscure more subtle fluctuations.

Cycle refers to the repeating sequence of an event that is "on" and then "off' such as a flowering episode followed by a nonflowering interval. Each repetition of the cycle may be variable in length (as in subannual flowering) or nearly equivalent (as in annual flowering). For some of the more complex annual flowering patterns, a larger cycle of one major flowering episode per year contains brief "pauses" of nonflowering intervals within it, which we refer to as the pulsed annual pattern after Oliveira et al. (1991). Monocarpic plants do not have repeating cycles at the individual level but rather only one reproductive cycle per lifetime (e.g., Tachigalia versicolor, Foster 1977; and some bamboo species, Janzen 1976).

Duration is the length of time a unit remains in a given portion of the cycle. In our classification, categories of duration for flowering episodes are brief (< 1 mo), intermediate (> 1 mo and < 5 mo), and extended (> 5 mo). The problem of resolution arises because a long census interval will overestimate the duration of flowering episode or nonflowering interval leading to an underestimation of the number of cycles per unit time. Daily observations are usually impractical, however, and a 2 wk or 1 mo census interval is commonly used in phenology.

Episode is the portion of the cycle during which the event is "on" such as flowering episode. Frequency is the number of cycles per unit time. We defined four arbitrary frequency classes based on an annual

time scale:

continual = always in flower with no or few brief interruptions; subannual = > 1 cycle per year;

Plant Phenology 159

annual = 1 cycle per year; and supra-annual = multi-year cycles.

Within the continual class, a continuous pattern means that there are no interruptions at all but this is not common at the individual and population levels. Within the supra-annual class, more frequent flowering patterns with 1 to 3 yr of flowering interspersed with 1 to 3 yr of nonflowering belong to the subclass alternate and infrequent flowering patterns belong to the subclass rare.

Interval is the portion of the cycle during which the event is "off' such as a nonflowering interval. At the population or guild levels this interval can also be referred to as a gap.

Regularity is the variability in length of cycles or portions of the cycles. Regular patterns, like annual flowering, have approximately equivalent cycle lengths and the "on" and "off" portions of the cycle tend to be consistent in duration from year to year. Irregular patterns, like subannual flowering, have variable durations of both the entire cycle and portions of the cycle. We are comparing quantitative methods for describing regularity (e.g., time series analysis and other methods such as those in Colwell 1974, Putz 1979, Raveh & Tapiero 1980, Stearns 1981).

Seasonal refers to the temporal association of an event with a recognizable climatic season. While an annual pattern is always seasonal in our data, the term annual refers to frequency (1 cycle/yr) not to seasonality. For example, supra-annual patterns may or may not have seasonal associations.

Date is the calendar time in days, months, or season of the year when the event occurs. It is an important reference point for relating plant phenology to external abiotic or biotic cycles. Date of flowering can be measured for first onset, or maximum, modal, or last flowering; each reflecting different properties of the plant's reproductive effort (Primack 1985).

Synchrony is the simultaneous occurrence of the same event in most or all of the units being considered (e.g., flowers on a tree or flowering trees in a population). Different quantitative measures of synchrony have been used (Primack 1980, Lack 1982, Augspurger 1983, Wright 1991).

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Issue Table of ContentsBiotropica, Vol. 26, No. 2 (Jun., 1994), pp. 117-232Front Matter [pp. ]The Effects of Past Fire Regimes on the Structural Characteristics of Coastal Plain Melaleuca vidiflora Sol. ex Gaert. Woodland and the Distribution Patterns of Epiphytes (Dendrobium canaliculatum R. Br., Dischidia nummularia R. Br.) in Northeastern Queensland [pp. 118-123]Wood Decomposition of Cyrilla racemiflora in a Tropical Montane Forest [pp. 124-140]A New Classification for Plant Phenology Based on Flowering Patterns in Lowland Tropical Rain Forest Trees at La Selva, Costa Rica [pp. 141-159]Indices of Habitat-wide Fruit Abundance in Tropical Forest [pp. 160-171]Wind Pollination of Neotropical Dioecious Trees [pp. 172-179]Pollinator Limitation of Fig Tree Reproduction on the Island of Anak Krakatau (Indonesia) [pp. 180-186]Characteristics of Feeding Guilds and Variation in Diets of Bird Species of Three Adjacent Tropical Sites [pp. 187-197]Bothrops asper (Viperidae) Snakebite and Field Researchers in Middle America [pp. 198-207]NotesArboreal and Terrestrial Mammal Trapping on Gigante Peninsula, Barro Colorado Nature Monument, Panama [pp. 208-213]Diurnal Insects Associated with the Flowers of Gomphocarpus physocarpus E. Mey. (Asclepiadaceae), an Introduced Weed in Australia [pp. 214-217]Insects Associated with Reproductive Structures of Cycads in Queensland and Northeast New South Wales, Australia [pp. 217-222]The Structural Role of Epiphytes in Ant Gardens [pp. 222-226]Measuring the Relationship between Floral Duration and Fruit Set for Hamelia patens (Rubiaceae) [pp. 227-229]Annual Waxy Bands on a Costa Rican Cactus [pp. 229-232]

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a new classification for plant phenology based on flowering patterns in lowland tropical rain forest...

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