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Box 5.2 Luxury Consumption in Epiphytic Bromeliads (Uwe Winkler and Gerhard Zotz)

Box 5.2 Luxury Consumption in Epiphytic Bromeliads (Uwe Winkler and Gerhard Zotz)

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Mineral Nutrition


Box 5.2 (continued)

phosphate. Entire plants were collected in regular intervals and total P, phytin

acid-P and inorganic P were determined as described in Alkarawi and Zotz


Tillandsia dyeriana


Phosphorus, mg g −1 dry weight


total P

inorganic P

phytin P













Days of fertilisation

The preceding figure shows means of 3 replicates and standard deviations

are given whenever larger than symbol size. Clearly, most of the initial foliar

P-concentration of c. 3 mg gDWÀ1 was present in the form of inorganic

phosphate (Pi, > 60 %), exceeding the proportion of P in phytic acid by

almost one order of magnitude. There was a steep increase in phytic acid

concentrations in the first month of the fertilization experiment, which also

led to a proportional change (17 % of total P in the form of phytic acid-P vs.

41 % in Pi). The increase in phytic acid continued for another month and

leveled off afterwards, while Pi continued to increase for the entire 4 months.

The relative changes in phytic acid concentrations exceeded those of both

total P and Pi, but in absolute terms inorganic phosphate increased four-fold


In conclusion, although phytic acid acts as a storage compound in green

tissue of this epiphytic bromeliad, particularly in the early stages of recovery

after nutrient deprivation, inorganic P is clearly the primary storage compound during luxury consumption.



5 Physiological Ecology

Reproductive Investment

Reproductive allocation is generally defined as the proportion of resources, e.g.,

biomass or nutrients, which are invested in reproductive organs or parts thereof,

e.g., seeds (Bazzaz 1996). Since most epiphytes face both frequent disturbance and

high abiotic stress (sensu Grime 1977), epiphytes are expected to allocate a large

proportion of their resource pools to support fecundity (Benzing 1990). Indeed,

published data indicate that up to 30 % of total plant biomass is invested in

reproductive structures (Benzing and Davidson 1979; Benzing and Ott 1981; Zotz

1999). Table 5.3 lists published details for two species of orchids and two species of

bromeliads along with unpublished data from nine species of orchids from Barro

Colorado Island, Panama (G. Zotz, unpubl.).

A particularly noteworthy observation is the enrichment of phosphorus in fruit of

Aspasia principissa by a factor of two with concentrations of almost 2 mg P gÀ1 dry

mass. Since the capsules account for about one-fourth of the total biomass of an

individual plant in this species, a single large fruit thus contains almost as much P as

all remaining plant parts together (Table 5.3). High nutrient allocation was also

found in the case of K, while N and Mg scaled approximately with fruit biomass in

this and other orchids. The data for bromeliads are too few to merit a detailed

discussion at the moment. Overall, the documented values for 13 species of

epiphytes exceed the reproductive investment in the majority of terrestrial

perennials and approach a level similar to that in many annuals (Hancock and Pritts


The shown data document substantial intraspecific variation. One possible

source of such variation is plant size, since reproductive allocation in plants is

frequently size dependent (Samson and Werk 1986). To date, there is a single study

addressing this question in vascular epiphytes. Surprisingly, reproductive allocation

in the orchid Dimerandra emarginata (expressed as relative investment of biomass

or nutrient elements such as N, P, K) did not vary with size (Zotz 2000). However,

while the investment during a given reproductive event was similar in smaller and

larger individuals, the frequency of reproduction varied substantially. Plants

>25 cm reproduce every year, while smaller individuals show an increasingly

lower probability (Zotz 1998): there is a 60-fold increase in the average annual

investment into fruits from smallest to largest reproductive individual.

Model calculations for pools and fluxes of the major elements P and N in mature

individuals of the tank bromeliad Vriesea sanguinolenta indicate that reproduction

is primarily limited by P-supply (Fig. 5.11, Zotz and Richter 2006). The data

suggest that the supply is so low that it takes two years to replenish P-pools to

allow renewed reproduction. It is probably not mere coincidence that 2 years is the

most commonly found interval between reproduction events in this epiphyte (Zotz

et al. 2005).



11.1 Ỉ 6.3

8.7 Ỉ 3.3


8.8 Ỉ 1.4

12.9 Ỉ 4.2

20.3 Æ 11.1

13.4 Æ 5.4

6.2 Æ 3.4


11.9 Æ 6.6

10.5 Æ 4.5





13.7 Æ 8

5.3 Æ 2.5


8.4 Æ 3.9

11.7 Æ 5.3

26.3 Æ 8.4

16.8 Æ 7.1

23.7 Æ 7.7

9.2 Æ 5.7


14.3 Æ 8.5

22.8 Æ 8.0



Data are means ặ SD (n ẳ 34 individuals) or means of two samples


Aspasia principissa

Brassavola nodosa

Camaridium ochroleucum

Catasetum viridiflavum

Caularthron bilamellatum

Dimerandra emarginata

Encyclia tampensis

Epidendrum difforme

Epidendrum nocturnum

Specklinia brighamii

Sobralia bletiae


Tillandsia streptophylla

Vriesea sanguinolenta




19.8 Ỉ 11.5

6.9 Ỉ 2.5


6.7 Æ 4

17.6 Æ 7.0

25.7 Æ 6.9

25.8 Æ 11.2

36.4 Æ 7.1

11.5 Æ 7.3


20.2 Æ 13.4

20.4 Æ 6.9





28.1 Æ 7.2

17 Æ 10.5


10 Æ 2.9

30.7 Æ 12.4

31.9 Æ 14.2

42.2 Æ 17.2

35.6 Æ 3.2

10.1 Æ 6.2


25.4 Æ 12.2

13 Æ 3.0





13.6 Æ 5

8.8 Æ 5.4


5.5 Æ 1.4

12.0 Æ 6.3

16.2 Æ 6.7

23.9 Æ 9.8

23.2 Æ 6.3

7.8 Æ 4.2


13.2 Æ 7.2

9.0 Æ 3.8



Benzing and Davidson (1979)

Zotz and Richter (2006)


Zotz, unpubl

Zotz, unpubl

Zotz, unpubl

Zotz, unpubl

Zotz, unpubl

(Zotz 1999)

Benzing and Ott (1981)

Zotz, unpubl

Zotz, unpubl

Zotz, unpubl

Zotz, unpubl

Table 5.3 Reproductive allocation (% resource in capsule compared to resource in entire plant) in nine epiphytic orchids and two epiphytic bromeliads


Mineral Nutrition



5 Physiological Ecology

Fig. 5.11 Nutrient pools (bold) and fluxes (italics) during the vegetative (V ) and the reproductive

state (R) of an epiphytic bromeliad Boxes represent different compartments of Vriesea

sanguinolenta plants. Figures in each square are nutrient contents in mg plant–1. Fluxes are

estimated from the different P or N pools in the vegetative compartments during the vegetative

and the reproductive state. Data were collected over 24 months. Net uptake was estimated as the

difference of the nutrient content of reproductive organs and the sum of all fluxes from vegetative

compartments. Reproduced with permission from Zotz and Richter (2006)


Mineral Nutrition



Associations with Fungi and Cyanobacteria

For ground-rooted plants, the importance of mycorrhizae for plant nutrient supply has

been demonstrated for a long time (e.g., Alexander et al. 1984). For epiphytes, there

are an increasing number of reports on the occurrence of mycorrhizae (Chap. 8), but

very little information on the functional implications. One of the few exceptions is a

study by Wu et al. (2011), who report that orchid mycorrhizal fungi in Phalaenopsis

roots significantly increased plant growth. The mechanism behind this observation

was not investigated. More conclusions can be drawn from another study in which

lithophytic Lepanthes rupestris was treated with fungicides (Bayman et al. 2002).

One fungicide which reduced the frequency of both pelotons and fungi in roots of

Lepanthes rupestris seedlings and juveniles increased mortality, whereas the fungicide that decreased the frequency of fungi in leaves, without affecting pelotons, did

not. These findings are consistent with a positive role for mycorrhizae and a negative

role for pathogens and/or endophytes. There is also the suggestion that saprobic

ascomycetes associated with the velamen of orchids may indirectly improve nutrient

access by decomposing the substrate outside the roots (Herrera et al. 2010). Taken

together, information on the functional role of fungal associates is scarce and does

currently not really suggest a very prominent role for nutrient uptake in epiphytes, not

least because of the low frequency of mycorrhizae among epiphytes. However, in

view of the accumulating evidence of an important role of the diverse groups of

fungal symbionts (mycorrhizal fungi, leaf endophytes, and dark septate endophytes)

for plant functioning in general (Kivlin et al. 2013), it is certainly worthwhile to have

another look at the relevance of the epiphyte-fungal relationship (Chap. 8).

There are a number of studies that document associations of epiphytes with

cyanobacteria, but their functional importance remains similarly unclear.

Cyanobacteria-containing coralloid roots are described for Zamia pseudoparasitica

(Benzing 1990), Nostoc and other cyanobacteria are regularly found in the velamen

of epiphytic orchids (Tsavkelova et al. 2003), and N-fixing bacteria were observed

in the phyllosphere of many Tillandsias (Brighigna et al. 1992) and in the tanks of

other bromeliad species (Fiore et al. 2007; Carrias et al. 2014).


Special Nutritional Modes Related to Animals

Animals may assist epiphyte nutrition either “voluntarily” or “involuntarily.” The

first case is given when, e.g., epiphytes trade carbohydrates and/or living space for

nutrients in myrmecophytic, mutualistic relationships and the latter when plants are

carnivorous. Treseder et al. (1995) have quantified the benefit that Dischidia major

(Rubiaceae) receives from housing ants of the genus Philidris, Dolichoderinae.

These ants frequently raise young and deposit debris such as dead ants, scavenged

insect parts, or feces in sac-like “ant leaves.” Using stable isotope analysis,

Treseder et al. (1995) estimated that almost 30 % of the nitrogen in tissue of

Dischidia major was derived from that debris. A direct demonstration of the

transfer of nitrogen from ants to the host plant under field conditions was achieved


5 Physiological Ecology

with 15N labeling experiments of ants and, respectively, the myrmecophytic fern

Myrmecophila sinuosa (Gay 1993) and the myrmecophytic orchid Caularthron

bilamellatum (Gegenbauer et al. 2012). Both species offer cavities as living space

(hollow rhizomes or pseudobulbs) and the orchid Caularthron bilamellatum also

carbohydrates in extrafloral nectaries. There are a number of additional

myrmecophytic species among epiphytes described in the literature (Fisher and

Zimmerman 1988; Huxley 1980), but a rigorous cost-benefit analysis of the tradeoffs in this interaction has not been tried with any of them.

Carnivorous epiphytic plants are mostly found in particularly wet, nutrient-poor

habitats (Benzing 1987). There are c. 1000 carnivorous species in the angiosperms,

distributed over 17 genera in 9 families (Barthlott et al. 1987). More than 5 % of

these are epiphytic, with 4 species of Lentibularia and 14 of Utricularia (both

Lentibulariaceae, Table 2.1), and c. 30 Nepenthes spp. (Nepenthaceae). Whether

the epiphytic bromeliad Catopsis berteroniana qualifies as carnivorous is

contested. It has been demonstrated that this species attracts and captures substantially more arthropods than other tank bromeliads (Frank and Omeara 1984).

Moreover, there are some features promoting carnivory such as UV reflection by

leaves, epicuticular waxes, or a central tank, but other requisites of true carnivory

are missing, e.g., prey digestion seems to be carried out exclusively by bacteria. To

distinguish such species from true carnivores, it has become customary to call them

“protocarnivorous.” It is largely unclear whether epiphytic carnivores have any

distinguishing characteristics from terrestrial congenerics. Benzing (1990) claimed

that there were no obvious differences between terrestrial and epiphytic members of

Pinguicula (Fig. 5.12) or Nepenthes, but provided no data to support this contention. The only study with pertinent data focused on Utricularia comparing biomass

allocation patterns in terrestrial, aquatic, and epiphytic species (Porembski

et al. 2006). Unfortunately, the inclusion of only a single epiphytic species limits

interpretation. Compared to six terrestrial species, epiphytic Utricularia quelchii

allocated twice as much biomass to leaves and 100 times more to traps, but less than

Fig. 5.12 Carnivorous

Pinguicula moranensis plant

on the trunk of a large oak tree

in a Mexican Pine-oak forest

at c. 2500 m a.s.l. Insert—

Detail of flowering

individuals (Photograph:

Valeria Guzman)


Mineral Nutrition


half to reproductive structures. Such large structural differences are likely to reflect

similarly pronounced functional variation, but the highly interesting system has not

been studied in this regard.


Intraspecific Variation in Hemiepiphytes and Facultative


Many of the comparisons made above between epiphytic and terrestrial plants

suffer from a potential phylogenetic bias. A possible way to avoid this bias is by

studying different ontogenetic stages of hemiepiphytes or epiphytic and groundrooted individuals of facultative epiphytes. In the former case, juvenile stages

completely depend upon canopy resources, while later stages with contact to the

ground can tap soil resources. The comparative study of plant water relations of

epiphytic and ground-rooted conspecifics usually demonstrates that—unsurprisingly—soil contact leads to improved water supply (Zotz and Winter 1994a, b;

Holbrook and Putz 1996; Liu et al. 2014). Nutrient supply, on the other hand, does

not show a similarly consistent trend (Table 5.4). While all epiphytic Clusia spp.

Table 5.4 Nitrogen concentrations (% dry matter) in leaves of epiphytic and ground-rooted

individuals of hemiepiphytes and facultative epiphytes


Clusia osaensis

Clusia peninsulae

Clusia rosea

Clusia uvitana


0.8 Æ 0.1 (4–40)

0.7 Æ 0.1 (4–40)

1.29 Æ 0.12 (18)

0.6 Æ 0.1 (13)


1.0 Ỉ 0.1 (4–40)

1.0 Ỉ 0.1 (4–40)

1.69 Ỉ 0.16 (12)

0.9 Ỉ 0.1 (25)






Clusia valerii



Ficus benjamina

0.6 Ỉ 0.1 (4–40)

1.68 Ỉ 0.3 (20)

1.1 Ỉ 0.1 (4–40)

1.73 Ỉ 0.2 (19)



1.6 Ỉ 0.4 (13)

1.33 Ỉ 0.16 (10)


Ficus pertusa

2.7 Ỉ 0.24 (5)

2.12 Ỉ 0.28 (5)


Ficus trigona

2.81 Ỉ 0.24 (5)

1.59 Ỉ 0.26 (5)






Anthurium acaule



0.84 Ỉ 0.15 (12)

0.87 Ỉ 0.15 (24)



Wanek et al. (2002)

Wanek et al. (2002)

Ball et al. (1991)

Zotz and Winter

(1994a, b)

Wanek et al. (2002)

Feild and Dawson


Schmidt and Tracey


Putz and Holbrook


Putz and Holbrook


Ball et al. (1991)

0.65 Ỉ 0.01 (6)

0.65 Ỉ 0.02 (6)


Ball et al. (1991)

1.87 Æ 0.07 (6)

2.33 Æ 0.15 (6)

2.44 Æ 0.1 (6)

2.78 Æ 0.14 (6)



Ball et al. (1991)

Ball et al. (1991)

Intraspecific differences were assessed with t-tests. Data are means Ỉ SD (n). Arrows indicate

significantly ( p < 0.05) lower (#) or higher (") concentrations in epiphytes (t-tests, p < 0.05);

n.s. not significant


5 Physiological Ecology

had significantly lower leaf N, nitrogen levels in leaves of epiphytic Ficus and

Schefflera tended to be higher or were statistically indistinguishable from those of

soil-rooted conspecifics. No significant difference was found in facultatively epiphytic Aechmea lingulata and Tillandsia utriculata (Ball et al. 1991). The finding

that both tank bromeliads have very low N concentrations irrespective of growing

site may result from generally low nutrient requirements or alternatively from

limited water and nutrient uptake by roots when growing on soil. In summary,

studies with hemiepiphytes and facultative epiphytes do not suggest that epiphytes

are generally more nutrient limited than ground-rooted species. Both plant groups

could make excellent systems for a better understanding of nutrient relationships in

tree canopies and should be used more often in future studies.


Photosynthesis, Carbon Gain, and Growth

Vascular epiphytes are autotrophs and engage in photosynthesis; there has been no

evolution toward a holoparasitic habit. In the plant kingdom, there are three major

types of photosynthesis, C3-photosynthesis, C4-photosynthesis (typically

characterized by a spatial separation of CO2 fixation via two different enzyme

systems, anatomically distinguishable by leaves with “Kranz anatomy”), and

Crassulacean acid metabolism (CAM), i.e., the temporal separation of nocturnal

uptake of external CO2 and actual fixation during daytime. Only two of these

possibilities, C3 and CAM, are found among epiphytes. (Whether unidentified

poikilohydric Tripogon species, which sometimes occur epiphytically (Porembski

2011), use the C4-pathway has not been determined.) Why are there no C4

epiphytes? One reason could be phylogenetic heritage—the major lineages with

C4 taxa (Poales and Caryophyllales) have hardly any epiphytic members

(Table 2.1). Second, C4 evolution is intimately associated with arid to semiarid

regions (Sage et al. 2011), which are spatially separated from the hotspots of

epiphytism. Finally, as pointed out by Sage (2004), C4 compensates for high rates

of photorespiration rather than helps against drought as such—consequently, even

in dry forests and savannas, which are dominated by C4 grasses, there is no

evidence of epiphytes using C4 photosynthesis (Mooney et al. 1989).

Crassulacean acid metabolism is prevalent among epiphytes not only in dry

vegetation; a substantial proportion of CAM species can be found even in wet

forests (Pierce et al. 2002b; Zotz 2004a). Orchids alone account for almost half of

all CAM species globally with c. 8000 taxa (Silvera et al. 2010). The only known

terrestrial orchids with CAM are in the Eulophiinae, an ancestrally epiphytic orchid

lineage (Bone et al. 2015). All other plant families together just add a comparable

number of species to the total (Smith and Winter 1996). Since a considerable

proportion of the latter are also epiphytic (e.g., in the Bromeliaceae), epiphytic

CAM species probably outnumber soil-rooted ones. (For a comparison of the

biomass of epiphytic and terrestrial CAM plants, see Box 5.3.) It is interesting to

note that the evolution of CAM and epiphytism are not necessarily tightly linked. A

phylogenetic study with Bromeliaceae found quite independent trends in individual


Photosynthesis, Carbon Gain, and Growth


clades in respect to the occurrence of CAM and epiphytism (Crayn et al. 2004).

However, while CAM is obviously not a prerequisite for the epiphytic lifestyle as

such, its occurrence seems essential for the spread into drier habitats—the more

xerophytic forms in this family are invariably CAM (Crayn et al. 2015).

Many physiological studies on epiphytes and hemiepiphytes specifically focused

on CAM, but there is also a considerable body of literature on leaf gas exchange of

C3 epiphytes. Although most research was done in the greenhouse or in the

laboratory, a number of field studies provide valuable insights into physiological

responses to the complex variation in abiotic conditions in situ (L€uttge et al. 1986;

Pierce et al. 2002a; Griffiths and Maxwell 1999; Griffiths et al. 1989; Zotz and

Winter 1994a).

Box 5.3 CAM Biomass in Epiphytes and Terrestrial Plants

Although it becomes increasingly clear that tropical forest canopies are the

global hotspot of CAM species in terms of diversity (Winter and Smith 1996),

this probably does not translate in a similar importance in terms of CAM

biomass at a local and global scale. Even in montane forests, where C3 and

CAM epiphytes can make up several tons per hectare (Table 9.1), they still

contribute less than 1 % to the total forest biomass (Edwards and Grubb 1977;

Tanner 1980). Since the proportion of CAM species decreases from the

lowlands to montane forests (e.g., Hietz et al. 1999; Griffiths et al. 1986),

the absolute biomass of CAM epiphytes may increase rather little with

altitude, but may actually decrease and drop to zero in upper montane forests

(Earnshaw et al. 1987). For example, in a montane forest in Mexico at an

altitude of 1980 m a.s.l., CAM species make up 8 % of the epiphyte flora, but

less than 2 % of their biomass, accounting for c. 6 kg haÀ1 (Hietz and HietzSeifert 1995 and Hietz, unpubl.). In the lowlands, CAM biomass was even

lower: Zotz (2004a) gives an estimate of c. 3 kg haÀ1 for the San Lorenzo area

in Panama.

Biomass estimates of CAM plants from arid areas may exceed these

figures by several orders of magnitude. For example, in the arid loma vegetation in northern Peru, the terrestrial CAM species, Tillandsia latifolia, alone

reaches more than 1600 kg haÀ1 (Rundel and Dillon 1998). Large cacti in

North American deserts or the succulent Karoo may reach similar values

(MacMahon and Wagner 1985; Milton 1990). This suggests that most CAM

biomass—at a global scale—is found in semi-deserts and other semiarid

biomes. This conclusion seems robust, even when taking into account the

larger land area covered by tropical and subtropical forests compared to semideserts (approx. a factor of 3, Olson et al. 1983). In addition, terrestrial CAM

plants from arid biomes may not only account for more standing biomass than

epiphytic CAM plants, but also show much higher potential productivity:


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Box 5.2 Luxury Consumption in Epiphytic Bromeliads (Uwe Winkler and Gerhard Zotz)

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