Oecologia (1990) 84: 544-552
Oecologia
9 Springer-Verlag 1990
A survey of vessel dimensions in stems of tropical lianas and other growth forms Frank W. Ewers ~, Jack B. Fisher 2, and S.-T. Chiu 1 1 Department of Botany and Plant Pathology, Michigan State University, East Lansing, MI 48824, USA 2 Fairchild Tropical Garden, 11935 Old Cutler Road, Miami, FL 33156, USA and Department of Biological Sciences, Florida International University, Miami, FL 33199, USA Received March 13, 1990 / Accepted in revised form May 30, 1990
Summary. Vessel dimensions (total diameter and length) were determined in tropical and subtropical plants of different growth forms with an emphasis upon lianas (woody vines). The paint infusion and compressed air methods were used on 38 species from 26 genera and 16 families in the most extensive survey of vessel length made to date. Within most stems there was a skewed frequency distribution of vessel lengths and diameter, with many short and narrow vessels and few long and wide ones. The longest vessel found (7.73 m) was in a stem of the liana (woody vine) Pithecoctenium crucigerurn. Mean vessel length for 33 species of lianas was 0.38 m, average maximum length was 1.45 m. There was a statistically significant inter-species correlation between maximum vessel length and maximum vessel diameter. Among liana stems and among tree + shrub stems there were statistically significant correlations between stem xylem diameter and vessel dimensions. Lianas with different adaptations for climbing (tendril climbers, twiners, scramblers) were similar in their vessel dimensions except that scramblers tended to have shorter (but not narrower) vessels. Within one genus, Bauhinia, tendril climbing species had greater maximum vessel lengths and diameters than tree and shrub species. The few long and wide vessels of lianas are thought to hydraulically compensate for their narrow stem diameters. The many narrow and short vessels, which are present in the same liana stems, may provide a high resistance auxiliary transport system. Key words: Lianas - Vessel diameter Water conductivity - Wood
Vessel length -
Vessel diameter and vessel length may be two of the most important parameters determining the efficiency of xylem conduction in plants (Zimmermann and Brown 1971; Zimmermann 1983). There is evidence that, at least in large woody plants, xylem conductivity may be Offprint request to: F. Ewers
an important factor constraining plant growth, development, and distribution in nature (Hellkvist et al. 1974; Schultz and Matthews 1988; Tyree 1988; Ewers 1985; Ewers et al. 1989). Vessel dimensions, which directly affect conductivity, have been correlated to extremes in growth form. A number of surveys have found that vessels of lianas (woody vines) are wider than in closely related trees (Ayensu and Stern 1964; Carlquist 1975; Klotz 1978; Van Vliet 1981; Bamber 1984; Ter Welle 1985; Ewers 1985). Similarly, Gartner et al. (in press) reported that in Jalisco, Mexico, naturally growing lianas had greater maximum vessel diameters than trees growing in the same dry hillside forest. However, there is a paucity of information on vessel lengths in lianas. Here we are referring to the total length of a vessel, not to the length of individual component vessel members (elements) for which there is much published information. Data on vessel member lengths have, in our opinion, limited value for functional or ecological studies since the entire vessel acts as the conductive unit. If an air bubble enters a single vessel member, the entire vessel becomes embolized and hence, nonconductive (Zimmerman and Brown 1971 ; Zimmerman 1983). Aside from our recent papers (Ewers and Fisher 1989a, b), vessel lengths have been published for only three lianas: two species of Vitis (Scholander 1958; Zimmermann and Jeje 1981; Sperry et al. 1987) and one species of Tetracera (Scholander 1958). In recent papers we investigated methods for measuring vessel lengths and diameters in woody plants (Ewers and Fisher 1989a) and, in six species of lianas, we examined within-stem and within-species variation in vessel dimensions (Ewers and Fisher 1989b). In the present paper we survey vessel dimensions in 31 species of tropical and subtropical lianas, and two non-woody monocotyledonous climbers, Asparagus falcatus and Luzuriaga latifolia. For convenience, these large monocots, although not truly " w o o d y " were classified as lianas. There is little previously published information to compare vessel dimensions in lianas with different structural adaptations for climbing, such as twiners (species
545 Table 1. Survey of vessel dimensions. For habit, SC = scrambler, SC/TEN = scrambling habit with occasional branch tendrils, SH = shrub, TEN = tendril climber, TR = tree, TW = twiner. For method, A = air, P = paint Taxon
Habit
Method
Xylem diameter (mm)
Vessel diameter (gm)
10
13
34
26
90
rain
~
Median
Vessel length (cm) max
~
Median
max
Dicotyledons Annonaceae Bhandari
Artabotrys hexapetalus (L. f.)
SC
P
5
3
27
TW TW TW
A A A
4.5 8.5 7
4 13 19
23 116 108
12 109 42
219 306 307
TEN
P
9
10
50
29
186
26
25
115
TEN TEN
A P
6 11
10 13
28 36
18 22
143 214
69
60
186 250
TEN TEN
A A
8.5 9
6 8
24 35
13 18
194 159
55 67
39 63
154 167
TEN TEN TEN TEN TEN TEN
A A A A A A
1.2 2 2.5 2.5 9 18
5 6 4
22 21 24
13 19 13
81 71 93
5 10
22 58
14 56
126 134
TEN TEN TEN TEN TEN TEN TEN
P P A P A P A
2.5 2.5 5 14 19 25.5 9
9 6 8 10 11
37 30 44 75 74
13 18 17 27 26
98 105 217 381 360
12
39
21
233
TEN TEN
P A
6 14
6 13
30 56
23 45
118 157
SC SC
A A
10 12
13
49
26
380
TW
A
12
16
64
29
401
57
62
SH SH
A P
5.5 6
8 9
27 31
25 18
75 92
3 5
3 3
TR TR TR TR
A P P A
11 11.5 11.5 16.5
13 9 9 13
48 51 57 55
38 47 60 44
115 117 113 132
10 30 29 15
5 35 25 10
83 85 75 100
TEN TEN TEN TEN
P P A A
3 3 4 4.5
8 6 6
29 20 20
16 12 14
146 124 182
7 13
5 5
55 55 184 157
Aristolochiaceae
Aristolochia gigantea Mart. & Zucc. A. maxima Jacq. A. veraguensis Duchartre
171 189 260
Bignoniaceae
Anemopaegmapuberulum (Sieb.) Miranda Arrabidaea corallina (Jaeq.) Sandw. stem I stem 2
A. podopogon(DC) A. Gentry stem 1 stem 2
Macfadyena (Doxantha) unguis-cati (L.) A. Gentry stem 1 stem 2 stem 3 stem 4
Mansoa allicea A. Gentry M. verrucifera (Schlecht.) A. Gentry Pithecoctenium crueigerum (L.) A. Gentry stem stem stem stem stem stem
1 2 3 4 5 6
Pyrostegia venusta (Ker-Gawl.) Miers Saritaea magnifica Dug. stem 1 stem 2
19 79
13 25
94 255 133 123 84 126
46
38
32 42 69 ]08 112 141
25 25 25 25 25 125
150 a 170 b 375
5 55
4 37
21 270
525 b
773 6258 153
Combretaceae
Combretum paniculatum Venten. stem i stem 2
199 170
Convolvulaceae
Argyreia nervosa (Burm. f.) Bojer
131
Fabaceae
Bauhinia aculeata L. stem 1 stem 2
34" 47"
B. blakeana Dunn. stem stem stem stem
1 2 3 4
B. corymbosa Roxb. ex DC stem stem stem stem
1 2 3 4
546 Table 1 (continued) Taxon
Habit
Method
Xylem diameter (mm)
Vessel diameter (gm) rain
~
Median
Vessel length (cm) max
f~
Median
max
B. fassoglensis Kotschy ex Schweinf. stem 1 stem 2 stem 3 stem 4 stem 5
TEN TEN TEN TEN TEN
A P P A A
3 3 3 3 3.5
10 10 6 6
24 37 42 23
18 22 29 14
210 215 233 213
27 11 9 23
10 5 5 5
65" 65" 45 73 270
SH SH SH
A P A
3.5 3.5 20
8 7 12
39 33 49
27 22 38
99 91 134
7 9 7
5 5 5
44 a 55 a 71
TR TR TR TR
A P P A
7 7 9 13
10 9 13 13
30 40 41 42
20 36 39 26
88 109 91 103
17 8 9 15
10 5 5 5
48 a 65 a 55 77
TEN TEN TEN TR SC/TEN TW
A A A A P P
7 9 11 12 12 6
7 6 9 10 9 4
51 24 43 48 48 14
43 17 25 38 39 10
185 226 211 144 133 189
17 37 26 11 12 37
10 30 13 10 5 30
SC/TEN SC/TEN
P P
4 6
10 9
42 66
27 56
161 193
TW TW
A A
6.5 7.5
10
29
20
176
TW TW TW
P A A
4.5 7 8
10 9 8
34 21 23
19 15 16
228 181 212
23
10
130 168 151
TW TW TW
A P A
4 4 7
8 6 6
25 20 33
15 14 21
208 207 222
43 27
37 12
160 a 87 a 194
SC SC
A A
11.5 11.5
7
27
21
107
TEN TEN TEN
A P A
1 1 3.5
4 7 4
26 34 17
13 20 12
128 87 249
TW
A
7
6
27
14
233
86
TEN TEN TEN
A A P
3 4.5 6
4
13
10
156
10
37
18
257
143 112 220
B. galpinii N.E. Br stem 1 stem 2 stem 3
B. purpurea L. stem stem stem stem
1 2 3 4 B. vahlii Wight & Arn. stem 1 stem 2 stem 3
B. variegata L. Dalbergia brownei (Jacq.) Benth. Derris scandens (Roxb.) Benth-
81 110 117 101 55 150
Hippocrateaceae
Hippoeratea volubilis L. stem 1 stem 2
30 38
20 20
100 220
Malpighiaceae
Maseagnia psilophylla (Juss.) Griseb. stem 1 stem 2
122+ 100
Peixotoa glabra Juss. stem 1 stem 2
Stigrnaphyllon cf. periploeifolium Juss. S. ellipticum (HBK) Juss. stem 1 stem 2 stem 3 Nyctaginaceae
Bougainvillea spectabilis Willd. stem 1 stern 2
32 43
Passifloraceae
Passiflora eoceinea Aubl. stem 1 stem 2 stem 3
16 10
5 5
52 a 45 a 179
Polygonaceae
Antigonon leptopus Hook. & Arn. Sapindaceae
Serjania polyphylla (L.) Radlk. stem 1 stem 2 stem 3
75
60
547 Table 1 (continued)
Taxon
Habit
Method
Xylem diameter (mm)
Vessel length (cm)
Vessel diameter (gm) min
2
max
Median
2
Median
max
Thunbergiaceae
Thunbergia grandiflora Roxb. stem 1 stem 2 stem 3
170 56 157
TW TW TW
A A A
8 10 12
10
42
26
301
TEN TEN TEN TEN
P P P P
4.5 14 16 24
10 12 12 12
45 50 63 79
23 27 27 35
179 233 287 337
SC SC SC
A A A
9 11 12
9
26
20
129
172+ 71
13
57
45
170
211
TW TW
A A
10
41
31
114
101 60
Vitaceae
Vitis rotundifoIia Michx. stem 1 stem 2 stem 3 stem 4
12 33 74 37
5 10 70 10
85 310 380 230
Monocotyledons Liliaceae
Asparagusfalcatus L. branches stem 1 stem 2 leader Philesiaceae
Luzuriaga latifolia (R. Br.) Poir. stem 1 stem 2
4.5 5
a For these stems vessel length data was from Ewers and Fisher (1989a) b Length data from Ewers and Fisher (1989b)
w i t h t w i n i n g t e r m i n a l shoots), t e n d r i l climbers, a n d s c r a m b l e r s (a m i x e d g r o u p o f species w h i c h t e n d to fall u p o n their s u p p o r t s a n d w h i c h m a y h a v e t h o r n s o r spines). R o o t c l i m b e r s were e x c l u d e d f r o m this survey. In a d d i t i o n to e x a m i n i n g different types o f lianas, in the p r e s e n t s t u d y we r e p o r t o n tree, s h r u b , a n d l i a n a species o f Bauhinia ( F a b a c e a e ) . T h e d a t a set includes, for seven o f the 38 species a n d f o r 16 o f the 86 stems, d a t a o n vessel l e n g t h e x t r a c t e d f r o m o u r p r e v i o u s p u b l i c a t i o n s (see f o o t n o t e s to Table 1). T h e vessel d i a m e t e r d a t a a r e all original. T h e objectives were to c o m p a r e vessel d i m e n s i o n s a m o n g v a r i o u s g r o w t h f o r m s a n d to d e t e r m i n e if there are inter-species c o r r e l a t i o n s b e t w e e n vessel length, vessel d i a m e t e r , a n d s t e m x y l e m d i a m e t e r . This s t u d y p r o vides g r o u n d w o r k for v a r i o u s o n g o i n g studies o f x y l e m s t r u c t u r e , f u n c t i o n , a n d e c o l o g y in lianas vis-fi-vis o t h e r g r o w t h forms.
B. galpinii
z
LU
rr 0,. 2 0 50
i- 6 0 z ill
0 n,uJ a.
2O
l
The sampled species (Table 1) were all growing outdoors at the Fairchild Tropical G a r d e n in Miami, Florida, except for Macfadyena unguis-cati, which was growing outdoors at the U S D A Subtropical Horticulture Experiment Station, Miami. Vessel length measurements were made in the spring and summers of 1985, 1986, and 1988. Vessel length distributions were determined by the paint or air method, (P and A in Table 1), with mean, median, and maxi-
2O
6'0
20
6'0
B. fassoglensis
2o L._~
50
N
. ~150
250
VESSEL
LENGTH
1(~0 (10 "2m)
I-,
20
Materials and methods
ii~'~
Aristolochia
5'0 VESSEL
150 DIAMETER
250
350
(,um/
Fig. 1. Frequency distributions for vessel diameter (light bars) and
vessel length (dark bars) for a stem of the shrub Bauhinia galpinii (stem 1 in Table 1), the liana B. fassoglensis (stem 4) and the liana Aristolochia maxima. Length distributions were not determined for Aristolochia. Maximum values (arrows) were greater in the liana than in the shrub. These are the best examples of stems from Table 1 with distributions that might be interpreted as bimodal
548 mum lengths determined for each stem. In some stems only maximum vessel lengths were measured, which is much faster than determining frequency distributions. Details of the paint and air methods, which produce similar results, are given in Ewers and Fisher (1989a). For each species the longest available unbranched stem segments were selected for study. In most but not all of these segments the leaves had abscised. In some cases, such as Bauhinia vahlii, which has regularly spaced short shoots along its main axis, small lateral branches could not be avoided. However, in every case we measured vessel length only along the main axis. For maximum vessel length determinations it was necessary to obtain stem segments longer than the longest vessel, but, as.we determined a posteriori, this was rarely a problem since vessel lengths were not as great as we had anticipated. Stem xylem diameter and vessel diameters were measured in the stem segment at one half the length of the longest vessel. This segment was fixed in FAA, transversely sectioned with a sliding microtome at 30 gm, and stained with safranin or safranin and fast green. A Nikon photostereomicroscope with transmitted light capabilities was used to prepare Kodachrome slides (diapositives) which were projected onto large sheets of white paper. Each vessel was marked on the paper as its inner diameter was measured with a ruler so that none were measured more than once. The projection resulted in spherical aberration errors of less than 1%. When a vessel was not circular in transverse view, the minimum and maximum diameters were averaged. For narrow stems, the diameter of every vessel in the stem was measured. However, wider stems often had well over a thousand vessels in cross sectional view. Rather than measure every vessel, we measured all the vessels in one or more sectors, with each sector having vascular rays for marginal boundaries and the pith and the vascular cambium as its inner and outer boundary, respectively. This avoided undue bias towards inner or outer vessels. When possible we sampled at least 100 vessels per stem. The above sampling procedure differs from that used in a previous study (1989b), where the diameters of only latex paint-filled vessels were measured. Since normal distribution of the variables was highly questionable, correlations were determined using Spearman's nonparametric coefficient of rank (Steel and Torrie 1980).
Results A s u m m a r y o f results for all the species e x a m i n e d is p r e s e n t e d in Table 1. T h e c o m m o n statistics o f m e a n a n d m e d i a n are given so t h a t o u r results c a n be m o r e easily c o m p a r e d to p r e v i o u s l y p u b l i s h e d surveys o f xylem a n a t o m y , a l t h o u g h such values for n o n - n o r m a l dist r i b u t i o n s s h o u l d be used with caution. M i n i m u m vessel lengths c o u l d n o t be d e t e r m i n e d b y o u r m e t h o d s . M o s t vessel length a n d vessel d i a m e t e r d i s t r i b u t i o n s were positively skewed, with m a n y s h o r t a n d m a n y n a r row vessels a n d few l o n g a n d few wide ones (Fig. 1). This is reflected b y the fact t h a t m e a n vessel length was greater t h a n the m e d i a n l e n g t h i n 9 6 % o f the stems e x a m i n e d in Table 1, a n d the m e a n s were always less t h a n 50% o f the m a x i m u m . Similarly, the m e a n d i a m e t e r was greater t h a n the m e d i a n d i a m e t e r in 9 9 % o f the stems e x a m i n e d , a n d the m e a n was closer to the m i n i m u m t h a n to the m a x i m u m in 100% o f the cases. F o r l i a n a species the overall m e a n o f the m e a n vessel lengths was 0.38 m ( S E = 0 . 0 5 ) , with a n average m e d i a n o f 0.26 m ( S E = 0 . 0 4 ) a n d a n average m a x i m u m o f 1.45 m (SE = 0.13). F o r all l i a n a species the m e a n o f the m e a n vessel diameters was 41 ~tm (SE = 3.9), with a n average
m e d i a n o f 26 g m ( S E = 3 . 1 ) a n d a n average m a x i m u m of 200 g m (SE = 13.2). T h e m e a n _ SE stem xylem diameters o f the s a m p l e d stems were as follows: all l i a n a species, 8.1_+0.6 r a m ; tendril climbers, 8 . 2 + 1 . 2 r a m ; twiners, 7.1_+0.6 m m ; scramblers ( i n c l u d i n g scramblers with occasional b r a n c h tendrils), 10.0_+ 1.0 m m . W i t h i n the genus B a u h i n i a the m e a n stem xylem diameters were: s h r u b s 7.4_+ 1.6 r a m ; trees, 11.2 _+ 1.1 m m ; tendril climbers, 5.2 -t- 1.9 ram.
Table 2. Spearman's coefficient of rank (rs) for various combinations of parameters. For ALL SPECIES, r~ is based upon the average value for each species in Table 1. For ALL LIANA STEMS and ALL TREE+ SHRUB STEMS, each stem was individually incorporated into the calculations. The differences in n were due to incomplete data sets for many stems. NS =not significant at 0.05 level of probability Parameters
n
Probability
25 25 38
NS NS
