IAWA Journal, Vol. 26 (1), 2005: 111-120

SEASONALITY IN CAMBIAL ACTIVITY OF FOUR FROM A MEXICAN LOWLAND TROPICAL RAINFOREST

Calixto Leon-Gomez1 & Arcadio Monroy-Ata2

SUMMARY

The rhythm of vascular cambial activity was studied in four species of lianas growing in a lowland tropical rainforest of Mexico. Cambial activity was determined by counting the number of layers of cells in the cambial zone. A greater number of layers was assumed to indicate greater cambial activity. In all four species (Machaerium cobanense, M.floribundum, Gouania lupuloides and octandrum) the cambium is active throughout the year. In three of the species (all but T. octandrum) cambial activity was significantly higher in the April-October rainy period than in the November-March dry period. Cambial activity in Trichostigma octandrum was not significantly associated with the wet or dry season. Key words: Cambial activity, successive cambia, tropicallianas, tropi­ cal rainforest.

INTRODUCTION

Most studies of cambial activity have been conducted in trees, with lianas only rarely being considered. The first studies of cambial activity in lianas, inc1uding seasonal changes in cambial activity, were on temperate species such as Vitis vinifera, V. riparia, inserta and Celastrus scandens, and the tropical Bougainvillea glabra (Esau 1948; Davis & Evert 1970; Pulawska 1973). Other workers have investigated seasonal changes in lianas by focusing on phenology (Croat 1975; Putz & Windsor 1987; Hegarty 1988; Opler et al. 1991). These studies show the dearth of information on lianas, and the need to understand the correlation between environmental factors and stern structure. In tropical and subtropical regions, correlation of cambial activity with seasons is not well understood for most species and there is often no c1ear separation of pronounced pe­ riods of activity and rest. In some tropical trees the cambium can remain active during the entire year, with peak periods correlated with rapid shoot extension. But in general, litde is known about the patterns of activity in tropical trees, inc1uding both the initiation and cessation of growth, due to the fact that very few studies have been conducted in tropical regions. As could be expected, little is also known about how lianas grow.

1) Departamento de Botanica, Instituto de Biologfa, UNAM, A. P. 70-233, Mexico 04510, D. E, Mexico. 2) Unidad de Investigaci6n en Ecologfa Vegetal, FES Zaragoza, UNAM, A. P. 9-020, Mexico 15000, D.E, Mexico. Associate Editor: Peter Gasson

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In many trees, growth rings suggest periodicity in increase in diameter of the stern, and though this phenomenon is little understood in tropical trees, growth rings are commonly observed. Growth rings are rare in lianas, making their age determination difficult. Therefore, this paper attempts to document the pattern of cambial activity in four species of from the tropical rainforest of the Los Tuxtlas region, Veracruz, Mexico. This area is mo ist year-round, with a peak during the single yearly rainy season. The temperature remains relatively constant throughout the year. The main objective of this paper is to test the hypothesis that lianas grow continuously throughout the year but with peaks in growth during the rainy season.

MATERIALS AND METHODS

Study area - Los Tuxtlas tropical biology field station is on the slopes of the Gulf of Mexico, in the southeast part of the State of Veracruz, with an elevation of 150 to 530 m, between 95° 04' and 95° 09' West longitude and between 18° 34' and 18° 36' North latitude (Lot-Helgueras 1976) (Fig. 1).The climate is warm-humid [Af(m)w"(i') following the classification of Köeppen modified by Garcfa 1981], with an annual pre-

95"10' 95"00'

18"40' 18"40'_

San Marlin Tuxtla ~ Volcano ~

18"30' 18"30'-

Santiago Tuxtla

18"20'_

o 5 10 I I km

Felipe Villegas 1L/1995 95"00'

Fig. 1. Map of the study area. The Tropical Biology Station is situated in southeast Mexico, at 25 km from the Catemaco-Montepio road.

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1400 2

1200

1000 E .§.. 800 ~ 600 ';;" "" 400

200

0 F M A M A o N 0 Month. 35 3 a 30 , - ~ --

15 J M A M A 0 Monlh Fig. 2 & 3. Precipitation and temperature graphs from the "Los Tuxtlas" station. The continuous line corresponds with the year 1998; the dashed line with 1999 and the dotted line with 2000. a: maximum temperatures; b: minimum temperatures. cipitation of 4700 mm (Fig. 2). The maximum temperature is 32.3 oe and the minimum temperature is 16.4 oe, with a mean of 24.3 oe (Fig. 3). material - The Iianas chosen for this study are characteristic of the primary forest of the region and reach basal stern diameters of up to 20 cm. The species inves­ tigated are Machaerium cobanense Donn.Sm. and M.floribundum Benth (Fabaceae), Gouania lupuloides (L.) Urban (Rhamnaceae) and Trichostigma octandrum (L.) H. Walt. () (Fig. 4).

Monlhs: F D Flowcring: FrUClifi al ion: •••• Vegelillivc growlh: ••••

Fig. 4. Species phenogram (Machaerium cobanense, M.floribundum, Trichostigma octandrum, Gouania lupuloides). The flowering norrnally occurs at the end of the dry period and the fruc­ ti/ication appears at the beginning of the rainy period. Machaerium cobanense is out of phase.

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Field work - The study took place from January 1999 through December 2000. For each species, two individuals with a stern diameter of 1-5 cm were collected monthly. A section of stern 2 cm long was taken from each individual and preserved in FAA (Sass 1958). When the sampies were less than 2.5 cm in diameter, transections were made of the entire stern. When the sampies exceeded 2.5 cm in diameter, they were sub-sampled in 6 to 8 transections containing vascular cambium and adjacent tissues.

Microtechnique - The xylem of these species is tough, especially in sterns of more than 1 cm in diameter, so the sampies were softened in a heated solution of 10% ethy­ lene-diamine for 30-60 min (cf. Kukachka 1977; Carlquist 1982), and embedded in glycol. Sections of 15-20 !Am were cut with a sliding microtome. Sections were stained with safranin-aniline blue (Johansen 1940).

Determination ofcambial activity - Cambial activity was determined by counting the number of layers or radial files of cells in the cambial zone. A greater number of lay­ ers of cells was assumed to indicate greater cambial activity (Paliwal & Prasad 1970: p. 337; Siddiqi 1991: p.179;Larson 1994: p. 597; Priya& Bhat 1999: p.183). Thetenns "cambium" and "cambial zone" are used in this study to designate the complete meri­ stematic zone including the fusifonn cambial initials and part ofthe phloem and xylem, of which the cells are enlarging but still capable of dividing, as described by Wilson et al. (1966). For each of the two individuals sampled monthly, from 4 to 8, but nonnally 6 counts of cambiallayers were made. For the transections of whole sterns, counts were made in four equidistant points, and for the subsectioned sterns, one count was made in each sub-sample. At-test was used to compare within-species differences between the rainy and the dry seasons for each species.

RESULTS Phenology and structure of the cambium The species studied are evergreen but have smaller crowns during the dry season. Machaerium ftoribundum, Gouania lupuloides and Trichostigma octandrum mainly in the January-April dry season. However, Machaerium cobanense in the rainy months of May to August (Fig. 2 & 4). All species nonnally fmit at the beginning of the rainy season, from March to July. Development of secondary xylem in the four species includes two types of cambia. Gouania lupuloides and Trichostigma octandrum have a 'nonnal' cambium in which the secondary xylem is produced as a continuous cylinder, whereas Machaeriumftori­ bundum and M. cobanense have successive cambia, in which the xylem alternates with concentric rings of phloem, corresponding to the Securidaca type of Carlquist (1988). In transection, the fusifonn and ray initials distinguish them from the cambial derivatives because of the abundance of periclinal divisions and thinner walls. The organization as viewed in tangential sections of the cambium varies for each species: no storying was observed in T. octandrum, while M. cobanense, M.ftoribundum and G.lupuloides have ray and parenchyma cells storied (Fig. 5).

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Fig. 5. Tangential stern seetions that show the longitudinal organization of xylem elements. - A : Machaerium cobanense. - B: M.jioribundum. - C: Gouania lupuloides. - D: Trichostigma octandrum. - M. cobanense, M. jioribundum and G. lupuloides have storied rays and paren­ chyma strands, while in T. octandrum there was no storying. - ap = storied axial parenchyma; r =storied ray. - Scale bar =200 ILm.

Annual variation in cambial activity In all four species, the vascular cambium is active all year round (Fig. 6 & 8), but the number of cambial celllayers is at its maximum during the rainy period. In Mach­ aerium cobanense, development is at its maximum of 4 to 6 celllayers during Febru­ ary to October with a mean number of layers of 3 to 4 the rest of the year (Fig. 8A). Machaeriumfloribundum presents a maximum of 4 to 7layers of cambium in July and August (Fig. 8B); Gouania lupuloides is at its maximum from April to October, with the formation of 6 to 8layers of cells, while from November to March only 4 to 5 layers are observed (Fig. 8C). In Trichostigma octandrum the number of layers of cambium fluctuates between 3 to 9 year-round (between different sampies) (Fig. 8D). Each species has a different mean number of celllayers, and during the rainy period these differences are most notable. Gouania lupuloides had a significantly greater

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Downloaded from Brill.com10/02/2021 04:16:13PM via free access Le6n-G6mez & Monroy-Ata - Cambial activity in lianes 117 number of cambiallayers, 6-8, in comparison with Machaeriumfioribundum, which has the smallest number of celllayers, 3-6 (p < 0.0001; Fig. 6).

Comparison oj cambial activity between the rainy and the dry period Given that seasonality was observed in the production of cambiallayers (Fig. 2, 3, and 8), means comparisons, using the t-test, were performed between the rainy period (April-October), and the dry period (November-March) for each species. The analysis was conducted to determine whether the differences observed in the data were correlated with environmental differences. In three species the results were strongly associated with seasonal fluctuations in water availability (Table 1). In Machaerium cobanense, M.fioribundum and Gouania lupuloides, cambial activity is significantly greater in the rainy season than in the dry season (p = 0.002566, P = 0.031199 and p = 0.000136). This is not the case for Trichostigma octandrum, which showed variation in cambial activity that was not significantly associated with the wet or dry season.

Table 1. Means eomparison test (Student's t) between the dry and the rainy periods, for eaeh speeies. The evaluated variable was the mean monthly number of eambiallayers; sampIe size: nl =5, n2 =7; degrees of freedom: d.g. 1 =4, d.g. 2 =6.

Speeies t exp. tO.005 = 1.81 P Machaerium cobanense 3.56** 0.002566 Machaerium floribundum 2.1 * 0.031199 Gouania lupuloides 6.15** 0.000136 Trichostigma octandrum 0.71 ns 0.248523 * =signifieant differenees; ** = highly signifieant differenees; ns = no signifieant differenees.

DISCUSSION

A common starting assumption for studies of cambial activity in tropical is that they are active year-round. This assumption was tested in the present study by testing for different levels of cambial activity between the rainy and dry seasons. Just one of the species studied exhibited more or less even cambial activity year-round, whereas the other three showed strong seasonality positively associated with rainfall. Machaerium cobanense and M.fioribundum have cambial zones with a mean number of 3-4 celllayers. Machaerium cobanense can be distinguished from M. fioribundum because it increases its cambial activity somewhat earlier in the rainy season (Fig. 7 & 8). Gouania lupuloides is the species with the greatest number of celllayers of the species examined. Its maximum number of cambiallayers occurs toward the end of the

Fig. 6. Cambial zone that shows the number and the width of the cambial cells. - A: Machaerium cobanense. - B: M.floribundum. - C: Gouania lupuloides. - D: Trichostigma octandrum. The left image shows the cambial status in the dry period (November to Mareh) and the right illustrates the cambial status in the rainy period (April to Oetober). - ez = eambial zone; P = secondary phloem; X =secondary xylem. - Scale bar =50 !-lm.

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70 60 B ~ 50 "c "...'"'c ... 40 "0- "0" 30 J: J: 20 10 0 9 10 8 9 10 ilmbial laycr> C;ullbinl 1lirel"l 50 60 D 50 C 40 ~ 40 '"'c "'"'c ... JO g 30 "0- ...0- e 20 !1: 20 "" 10 10 0 0 2 3 4 5 6 7 H 9 10 2 4 5 6 7 8 9 10 Cambial laycr, Cnmb",lla)cr,

Fig. 7. Frequency average in the number of cambiallayers in four lianas. - A: Machaerium cobanense. - B: M. jioribundum. - C: Gouania lupuloides. - D: Trichostigma octandrum. - G. lupuloides exhibits a nonnal distribution with the highest number of layers and the other species show a frequency based on a lower number.

6 (, "~ A t 5 <> 5 B ">. >. .2 4 4 -;;; " :ö 3 :ö'" 2 E E " I " I 0 0 .~ ~ J I' M A M J J J ~ 1 A :VI J J 1\ S 0 r.; D MOnlh, Month, 8 6 7 C D '"'-<> c. 5 >. 6 ...... 2 5 .2" 4 -;;; 4 -;;; .1 :ö 3 :ö 2 E 2 § I U" I Ü 0 ~ 0 J I' M A M J J A 0 :-: D J I' M A M J J 1\ 0 0 Month, Month,

Fig. 8. Distribution patterns of the monthly mean number of cambiallayers during an annual cycle. - A: Machaerium cobanense. - B: M. jioribundum. - C: Gouania lupuloides. - D: Tri­ chostigma octandrum. The cambial activity is continuous throughout the year, nevertheless the number of layers is lower in the dry period (November-March) than in the rainy period (April-October). Trichostigma octandrum does not show seasonality.

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The constant temperature at the study site means that temperature variation is unlikely as a factor influencing cambial activity in the species examined. However, rainfall does vary significantly at Los Tuxtlas and appears to be of great importance in influencing cambial activity (cf. Creber & Chaloner 1990; Priya & Bhat 1999). In effect, marked seasonality between rainy and dry season is associated with significantly greater cam­ bial activity in three of the species studied (all but T. octandrum). Avila et al. (1975) suggest that cambial rhythm is genetically controlled and, in many plants, its rhythm is determined by water availability. The observations and analysis presented here suggest that lianas from tropical areas with more or less constant temperature and variable rainfall show activity year-round, with a significant increase during the rainy periods.

ACKNOWLEDGEMENTS

The first author thanks the Direcci6n General de Asuntos deI Personal Academico (DGAPA) and the Instituto de Biologfa of the Universidad Nacional Aut6noma de Mexico (UNAM), for their financial support of this research and for a doctoral thesis grant. We thank the Estaci6n de Biologfa Tropical "Los Tuxtlas" for support in field work. Also, we are especially thankful to Dr. M. E. Olson for his valuable corrections and translation to the final manuscript. We appreciate the critical revisions to the initial document by Dr. G. Angeles and Dra. T. Terrazas. Finally, we gratefuly acknowledge the helpful comments of two anonymous reviewers.

REFERENCES

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