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I. Introduction

Tropical forests harbor a particularly large diversity of bryophytes (mainly mosses and liverworts). The Neotropics alone are home to some 4,000 species of bryophytes, which represents about a quarter of the global species number (Gradstein et al. 2001). The majority of species grows epiphytically on live stems and branches of trees and shrubs, although a variety of other substrates are also used, -e.g. leaves (these epiphytes are referred to as epiphylls, Ruinen 1953), rocks, decaying wood, or termite mounds (Pócs 1982). Lowland rainforest floors are virtually devoid of bryophytes, probably due to high litter input, but subalpine forests can boast fully moss-covered soils (Wolf 1993) and terrestrial mosses can also be found in alpine bogs (Bosman et al. 1993) and in drier regions as a component of biological soil crusts (Belnap and Lange 2001; Godínez-Alvarez et al. 2012).

Bryophytes (and lichens) show a dramatic increase in abundance (e.g. Frahm 1990a; Wolf 1993) and diversity (e.g. Seifriz 1924; Pócs 1982; Gradstein and Pócs 1989) as one moves uphill away from the tropical lowlands. This increase is particularly noticeable above 1,000 m elevation and often reaches a maximum in upper montane forests around 3,000 m, while decreasing again above the treeline (Grau et al. 2007). For example, the “bryomass” in the Uluguru mountains in Tanzania increased from 1 kg ha−1 at 20 m elevation to 440 kg ha−1 in the ‘mossy’ forest at 2,100 m. (Frahm 1990a). Not surprisingly then, the impact of bryophytes on ecosystem function, particularly on hydrology (Pócs 1980; Hölscher et al. 2004) but also on nutrient cycling, is highest in montane systems (Hofstede et al. 1993; Nadkarni et al. 2004; Clark et al. 2005). For example, it has been extrapolated by Pócs (1980), that epiphytic bryophytes in an elfin forest may intercept more than 40,000 l of precipitation ha−1 year−1. Leaching and decomposition of bryophyte organic material result in a pulsed release of nutrients after rehydration of dry mosses. Coxson (1991) estimated an efflux of 80 kg K ha−1 year−1 in a tropical montane rainforest on Guadeloupe.

This ecological importance contrasts strongly with the availability of information on the ecophysiology of this plant group in the tropics. Just a handful of studies has addressed the ecophysiology of tropical lowland bryophytes, focusing on desiccation tolerance (Biebl 1964; Johnson and Kokila 1970), temperature tolerance (Biebl 1967), or photosynthetic light response and related functional traits (Waite and Sack 2010) and photosynthetic light, water, and temperature responses (Wagner et al. 2013). For bryophytes from the tropical montane zone the situation is somewhat better, with a number of published studies on CO2 exchange (Frahm 1987a, b; Lösch et al. 1994; Zotz et al. 1997; Wagner et al. 2013), water relations (Biebl 1964; Proctor 2002) and temperature responses (Lösch and Mülders 2000). For upper montane cloud forest the information is very scarce again (Lösch et al. 1994; Lösch and Mülders 2000; Romero et al. 2006), though an interesting recent contribution addresses altitudinal patterns, including lowland and upper-montane sites (300–2,200 m elevation), in various ecophysiological parameters (δ13C, N:P; Waite and Sack 2011a, b). We restrict this review to these moist forest types, simply because no ecophysiological data are available for bryophytes in other tropical ecosystems such as páramos, grasslands, dry forests or deserts. The dearth of information on mosses caused us to include some studies on tropical forest lichens in this review. This seems appropriate since both groups share major characteristics of their physiology, in particular their size and poikilohydric habit (Green and Lange 1994). Even after combining studies with lichens and mosses, the current data basis is thin, yet it is substantial enough to allow some major conclusions.

Several of the available studies focus on the same question: what is the physiological basis of the described gradient in diversity and abundance with altitude? Possible explanatory factors are reviewed in Frahm (1987a, b):

  1. 1.

    Increase of irradiance with increasing altitude

  2. 2.

    Decrease of temperature with increasing altitude

  3. 3.

    Increase of precipitation with increasing altitude

  4. 4.

    Direct influence of fog and dew in tropical montane forest

Tested in isolation, all these suggestions can be partly rejected. For example, shady locations in montane rainforests may still have lush bryophyte cover. On the other hand, even in wet tropical lowland rainforests where monthly rainfall always exceeds 100 mm, bryophytes are mostly rare. In fact, globally there is hardly any correlation between precipitation and bryophyte biomass (Lakatos 2011), as counterintuitive as this may be. On the other hand, air humidity correlates with moss cover within the tropical lowlands up to 650 m a.s.l. and highlands from 1,000 to 3,500 m a.s.l. (Karger et al. 2012). Also, in rare lowland situations where cool air accumulates at night and bryophytes are moistened by fog on most mornings, as in the newly described ‘lowland cloud forest’ in the Guyana Basin (Gradstein et al. 2010), bryophytes are quite abundant in the forest canopy. This combination of environmental conditions, also found in bryophyte-rich tropical montane forests and temperate rain forests, appears to be particularly favorable for bryophyte growth. Such observations lend support to an ecophysiological explanation for the lack of bryophytes in tropical lowland rainforests originally proposed by Richards (1984). He suggested that the low bryomass in the lowlands is due to high temperatures at night causing high respiration rates and large nocturnal carbon losses, which cannot be compensated during the day, when photosynthesis is restricted either by low light levels (during rainstorms and in the forest understory) or, in high-light conditions, by fast drying (Fig. 15.1).

Fig. 15.1.
figure 1

Diel gas exchange courses of two bryophyte species of similar life form from a canopy (left, redrawn from Zotz et al. 1997) and a forest understory species (right, Westerman and Zotz unpublished data) in a lower montane rain forest (Fortuna, Panama, see section “The physical setting”). From top to bottom: net CO2-exchange (NP, nmol g−1 s−1), water content of the shoots (WC, %DW), air temperature (T, °C) and photon flux density (PFD, μmol m2 s−1). Note how in the understory the moss is active all day, with NP restricted by very low PFD, while in the canopy NP is restricted by low WC with no activity for several hours around noon. Activity after an afternoon rain is low (due to low PFD and possibly supersaturation). Note the 20-fold difference in the scales of the PFD axes in the lower right panel (dashed line scaled on right-hand y-axis)! Similar NP rates in spite of this are due to different maximum rates of the two species.

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In the following sections the current understanding of the physiological ecology of tropical bryophytes will be reviewed. We start with a brief description of particularities of the physical setting in the tropics and continue by discussing what is known about carbon relations of tropical bryophytes, or lichens if information on bryophytes is lacking completely. The problems described by Richards (1984) are a recurrent theme: the timing of hydration, light limitation and respiratory losses at high night temperatures. Considering the potentially dramatic impact of climatic changes on tropical ecosystems (e.g. Solomon et al. 2009; Wright et al. 2009; Lewis et al. 2011) we will end our contribution with a short outlook on the particular fate of tropical non-vascular epiphytes.

II. The Physical Setting

Physiologically, tropical bryophytes probably do not differ fundamentally from bryophytes elsewhere – or rather, the data basis is too thin to decide whether they do (Proctor 2002; Waite and Sack 2010). Yet the tropical environment sets particular limits and requirements for bryophyte functioning and growth. Tropical climates are not uniform, which is reflected in the range of vegetation types in the lowland tropics from, e.g., wet rain forests to savannahs to deserts. Mountains introduce elevational cooling trends, which also affect precipitation regimes, adding additional vegetation types. Tropical climates differ from all non-tropical climates in one respect: diurnal fluctuations in temperature are generally more pronounced than seasonal ones. Seasonal changes in precipitation, on the other hand, are common. Noteworthy, an extended dry season may exclude bryophyte taxa with limited desiccation tolerance (see sections “Effects of hydration and desiccation on carbon balance” and “Desiccation tolerance: desiccation duration and intensity”). Thus, a “tropical” site is not necessarily a wet and/or warm site, so that the local occurrence of a tropical bryophyte species may well be restricted by drought in a coastal desert or by frost in the páramo. Apart from these large-scale gradients in environmental conditions, there is predictable variation at a smaller scale, in particular along the vertical gradients of light, humidity, wind speed and temporal variability inside a forest. This temporal variability, daily oscillations in light and temperature in particular, is more pronounced in the upper strata of a forest than in the understory (Zotz and Winter 1994).

This chapter on tropical bryophytes focuses on wetter vegetation types, moist or wet lowland rainforests and montane rain or cloud forests. The following paragraph summarizes the general physical setting of tropical wet climates (Richards 1996). The most striking feature of the tropics is the high humidity, which is generally 60–80 % (or even higher) during the day and 95–100 % during the night. Within 10° latitude of the equator the mean annual temperature range is between 24 and 28 °C in the lowlands, while temperatures over 35 °C are rare due to the cooling effect of evapotranspiration. The decline of temperature with altitude differs among regions. For example, in Costa Rica the decline is highest up to the cloud base with 1.2 °C per 100 m, lowest within the clouds and moderate above the cloud belt (0.6 °C per 100 m). By definition, annual precipitation in the wet tropics is high, ranging from 1,700 to >10,000 mm, with rainfall >3,000 mm, as found in western Colombia or New Guinea, considered as ‘super wet’. In most cases there are two rainfall peaks annually, and north of 10° only one peak. The dry season (<100 mm month−1) lasts typically less than 3 months and is irregular from year to year in the wet zones. In the super wet zone, dry periods are rare very short (less than a few weeks) and occur infrequently and irregularly.

Detailed climate data from lowland rainforests are readily available (e.g. from research stations like La Selva in Costa Rica or BCI in Panama), while data from montane habitats are rarer. For bryophyte ecophysiology, the most relevant information is on the microclimate directly at the bryophyte growing site and we will here present such data from a lower montane rainforest in western Panama (Fortuna, ca. 1,100 m; Zotz et al. unpublished). This is the locality where most of the available gas-exchange data for montane bryophytes and especially lichens have been collected (Zotz et al. 1998; Lange et al. 2000, 2004). The data presented here were recorded in situ for 14 days from September 18 to October 2, 1994.

Sunlight (measured as photosynthetic photon flux density, PFD) incident on the canopy exceeded 3,000 μmol m−2 s−1 on 5 of the 14 days, with an absolute maximum of 3,245 μmol m−2 s−1. Daily integrated PFD above the forest canopy ranged from 15 to 48 mol m−2 day−1, averaging 29 mol m−2 day−1. Although surprisingly high at first glance, such values are not unique. For example, Körner et al. (1983) report peak values during sunny spells in overcast situations of >2,800 μmol m−2 s−1 from Pinadaunde Valley, New Guinea (ca. 3,500 m elevation), and maximum PFD values >2,500 μmol m−2 s−1 are also regularly reported from the lowland sites of La Selva (Costa Rica) and BCI (Panama): on 24 and 14 %, respectively, of all days during 1993–1995 (Sources: http://www.ots.ac.cr/en/laselva/metereological.shtml and http://stri.si.edu/sites/esp/). Not surprisingly, PFD within the forest differs drastically from such high values. In the understory in Fortuna, daily maxima exceeded 20 μmol m−2 s−1only during brief light flecks (Fig. 15.1).

Diurnal changes in air temperature averaged 6.9 ± 1.3 °C, with night temperatures of 16–17 °C and peaks of up to 26 °C around noon. Air temperature gradients within the forest were negligible, but temperature is buffered inside the forest compared to the forest edge (Fig. 15.2).

Fig. 15.2.
figure 2

Diel course of hourly temperature means at ca.2 m height in Fortuna, Panama, on July 7th 2011 (Wagner et al. unpublished data). Dashed line: forest edge. Solid line: inside forest.

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Although no moss was measured, temperature measurements of a lichen thallus on a branch at ca. 3 m height at the forest edge during the same period should also be instructive for mosses. Maximum temperatures reached up to 36°, but averages were only slightly elevated compared to ambient (+1.2 °C).

While overall precipitation was quite high (ca. 100 mm in 14 days), rainless periods were rather long with average intervals between rain events (>1 mm) of 23 h. However, ‘lateral’ precipitation in the form of mist or fog, which is not captured by traditional rain gauges, occurred nearly every morning and sometimes during the day as well. Cavelier et al. (1996) found fog interception contributing between 2.4 and 61 % of the total water input depending on altitude in tropical Panama. Early-morning air was invariably saturated with water vapor and even around noon the relative humidity was still 75–80 %.

Growing close to living or decomposing substrate, CO2 concentrations in the phylloplane of mosses and lichens may deviate substantially from ambient conditions (Tarnawski et al. 1992). This was also the case in Fortuna, where this difference amounted to about 100 ppm (Table 15.1). We also noticed diurnal variation, with predawn CO2 concentrations [CO2] in the air and in mosses being consistently higher, by ca. 30 ppm, than those measured in the morning (Table 15.1).

Table 15.1. CO2 concentrations (ppm) in the air and within the phylloplane of mosses, growing on living and dead wood in the lower parts of the forest measured before sunrise (5 am) and at 9 am on Sept. 30, 1994 in the lower montane rainforest of Fortuna, Panama (ca. 1,100 m a.s.l.)
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III. The Carbon Balance of Tropical Bryophytes

The most accepted explanation for the generally observed altitudinal trend in bryophyte abundance in the tropics involves environmental limitations for obtaining a positive carbon balance (Richards 1984; Frahm 1987b; Zotz 1999). Photosynthetic response curves and diel carbon balances have been determined for a small number of tropical bryophytes (see Table 15.2). For tropical lowland species, only a few published light response curves are available (Waite and Sack 2010), so that in the following discussion we also include the few data on lichens for the lowland situation (Zotz and Winter 1994; Zotz et al. 2003).

Table 15.2. Maximum rates of net photosynthesis (NPmax), rates of dark respiration (RDmax), and light compensation points (LCP) for a suite of tropical bryophytes. All measurements under optimum water content and average normal temperature of the study site.
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A. Growth

Information about growth and primary production of tropical bryophytes is scarce. There is only one study on growth and net production of tropical montane bryophytes (Clark et al. 1998). They divided bryophyte samples into two subgroups based on life forms (Mägdefrau 1969, 1982). Mass accumulation was slightly higher in turf-, weft- and mat-forming bryophytes (24.0 % year−1 on average) compared to pendants, fan- and tail-forming species (15.5 % year−1). Average net primary production was estimated at 122 g m−2year−1 for the pendant group and 203 g m−2year−1 for the turf group. These estimates were rather low compared to other ecosystems where bryophytes are abundant (summarized by Clark et al. 1998).

B. Maximum Carbon Exchange Rates

Light response curves of a range of tropical bryophyte species demonstrate rather low ratios of maximum net photosynthesis (NPmax) to dark respiration (Rdmax), on average 3.7. It ranged from <1 (i.e. dark respiration rates exceeding maximum photosynthesis rates) to >10 (Table 15.2). The NPmax/Rdmax ratios of leaves of vascular plants usually are around 10 (Larcher 2001). Although these relatively high respiration rates in bryophytes are not specific to the tropics (Green et al. 1998; Pannewitz et al. 2005), the consequences for diel carbon balances may be particularly pronounced in tropical lowlands because of the unfavorable timing of hydration and metabolic activity (see section “Effects of hydration and desiccation on carbon balance”). An NPmax/Rdmax ratio of c. 4means that even under the (unrealistic) assumption of saturating light conditions, optimal water content, and optimal temperature throughout the day one fourth of the carbon gain is lost during the 12 h of the night. This assumes that dark respiration at night equals dark respiration during the day, though this is not necessarily true in higher plants (Amthor 1995), while for bryophytes it has not been tested as far as we know. Since conditions are mostly far from optimal, as we will discuss below, even in montane forests (and for lowland lichens, see Zotz and Winter 1994), observed diel carbon balances are often negative (Zotz et al. 1997). Logically, longer-term carbon balances have to be positive if species occur at all. The high relative losses imply, however, that balances are close to unity. It is critically important for the entire argument that Rd is not simply regulated by substrate availability, which could indeed be shown for lichens in the temperate zone (Lange and Green 2006): the nocturnal respiration of two chloro- and one cyanolichen studied in their natural habitat was not affected by preceding diurnal net photosynthesis, so the amount of carbohydrates available as substrate was less important than other environmental conditions.

C. Diel Balances

Diel carbon balances can be calculated from frequent gas exchange measurements on bryophytes in situ over a 24-h period. Variability between days can be substantial and to quantify longer-term carbon balance requires a very large number of measuring days (Bader et al. 2010). Still, even a limited set of days can indicate how diel balances depend on environmental conditions and can reveal typical patterns for a given climate zone (e.g. Lange et al. 2004).

Bryophytes in a lower montane rainforest (Fortuna, see section “The physical setting”) lost, on average, about 60 % of the carbon gained on a given day during the subsequent night (Zotz et al. 1997). In the lowlands, proportional respiratory losses may be higher, but this assumption has not been tested for bryophytes. The foliose lichen Leptogium azureum from lowland Panama had a negative integrated diel carbon balance on 7 out of 13 days studied during the wet season (Zotz and Winter 1994). Two days were studied in the dry season and both were negative. A similar situation was found for another lowland lichen, Parmotrema endosulphureum, with only three positive diel balances out of seven measured days and an average nocturnal loss of 90 % of the daily gains (Zotz et al. 2003). This pattern was not due to absolutely low carbon gains, which were comparable to those of central European bryophytes in their most productive season (Zotz and Rottenberger 2001), but due to high nocturnal losses. In lower montane rainforest, lichens were found to lose less of their daily carbon gain at night (averages for 5–15 days between 59 and 94 % for different species), though negative diel carbon balances frequently occurred in some species (Lange et al. 2000, 2004). For comparison, the epilithic lichen Lecanora muralis from Europe had a negative diel carbon balance on 25 % of its active days measured in 1 year, and lost on average 57 % of the daily gains at night (Lange 2003).

IV. Effects of Hydration and Desiccation on Carbon Balance

As poikilohydric organisms bryophytes equilibrate more or less rapidly with external moisture conditions. Physiological activity ceases reversibly when shoots become too dry, whereas abundant external water limits photosynthesis, but not respiration, by increasing the diffusion resistance for CO2 (Proctor 1981, 1990). Water relations thus prominently affect carbon relations, while also setting the requirements for desiccation tolerance. The effects of moisture regimes on bryophyte (and lichen) physiology include at least five dimensions (last four from Norris 1990): (1) time of day of hydration, (2) hydration duration (activity time), (3) desiccation-rehydration frequency, (4) desiccation duration, and (5) desiccation intensity. In the following sections we will apply this framework on bryophytes in tropical montane cloud forests and lowland rainforests. More in-depth reviews of bryophyte hydration dynamics and desiccation tolerance can be found in, e.g., Proctor et al. (2007a) or Green et al. (2011).

A. Timing of Hydration

The timing of hydration during a day has strong implications for the balance between photosynthesis and respiration. A “typical” day in the tropical lowlands includes rain in the afternoon (continental regions) or late at night (maritime regions) (Richards 1996). For bryophytes this is unfavorable, because they are moist and physiologically active during much of the night. As a consequence much of the carbon gained during the preceding day is respired, especially since temperatures generally remain high during the night. If the following day is sunny, the bryophyte will then usually dry out before noon, thus missing out on the favorable light conditions (Zotz et al. 1997). In contrast, morning rain or fog increases the diel carbon balance, because high light levels at midday may coincide with optimal shoot water contents for photosynthesis. For the tropical lowland lichen Parmotrema endosulphureum the only day (out of seven) with a highly positive carbon balance occurred when thalli were dry all night and a rainstorm burst them into life after sunrise (Zotz et al. 2003). On the other hand, for corticolous lichens, a common life form in the lowland forest understory, late-morning dew on stems still cool from the night may be a significant extra water source and favorably timed relative to the midday light conditions (Lakatos et al. 2012).

Morning fog is the default situation in montane cloud forests, where rising air condenses into clouds while passing these forests. This allows carbon gain in the morning, although on sunnier days drying is often complete before the highest light conditions at midday, as found for a range of lichen (Lange et al. 2004) and bryophyte species (Zotz et al. 1997). Late-afternoon rain and fog are also common, hence nocturnal respiratory losses can be considerable in these ecosystems as well (Fig. 15.3), but may be lower than in the lowlands because of the lower temperatures (Zotz et al. 1997). Morning fog also appears to play an important role in maintaining a high bryomass in the rare tropical lowland cloud forest (Gradstein et al. 2010).

Fig. 15.3.
figure 3

Diel gas exchange courses (same day) of a pendant (left) and a cushion species (right), both from the forest edge in a lower montane rain forest (Fortuna, Panama, see section “The physical setting”). From top to bottom: net CO2-exchange (NP, nmol g−1 s−1), water content of the shoots (WC, %DW), air temperature (T, °C) and photon flux density (PFD, μmol m2 s−1). Arrows indicate a heavy rain event (Redrawn from Zotz et al. (1997)). Note the fast drying of the pendant species (left) and the supersaturation depressing NP in the cushion in the morning (right).

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The timing of hydration may also be important in the context of intrinsic circadian rhythms in physiological processes. An internal clock exists in plants, including mosses, which causes diurnal fluctuations in net photosynthesis even when the plants are kept in constant light (Hennessey and Field 1991; Holm et al. 2010). Such fluctuations serve to increase metabolic efficiency by anticipating daily fluctuations in environmental conditions, in particular sunlight and potentially also hydration. The ecological relevance of such internal fluctuations, possibly interacting with fluctuating moisture conditions to affect carbon balances and stress responses, is unknown but may be worth investigating.

B. Activity Time

Many bryophytes spend most of their lives in a dry and inactive state. Carbon gain and growth are restricted to periods of sufficient hydration, and capturing and storing moisture are crucial abilities for bryophytes. Open life forms like pendants and fans are better suited for capturing moisture, while more compact forms like cushions, turfs and mats are generally better at water storage (Bates 1998; Kürschner et al. 1999). Pendant species are conspicuous in many tropical montane forests, where they can capture water from the frequent passage of clouds (Proctor 2002), although physiological activity before drying out again is short (in the order of a few hours, depending on conditions; Zotz et al. 1997, Wagner, unpublished data). In such species, carbon gain is obviously limited by low water content, in contrast to cushions in which carbon gain is frequently limited by supersaturation (Zotz et al. 1997; Fig. 15.3), so that a cushion reaches its highest rates of photosynthesis later than the pendant species (Fig. 15.3). A rain event in the afternoon can allow additional carbon gain in pendant species, while in cushions it may further reduce net CO2 uptake due to supersaturation (Fig. 15.3).

Some bryophytes are able to hold large amounts of water; we have recently measured water contents ~7,000%DW in cushions of Octoblepharum pulvinatum directly after tropical rain events (T. Reich and S. Wagner, unpublished data). The pendant Phyllogonium fulgens can hold up to ~2,700%DW (Zotz et al. 1997), which agrees with reports from another pendant, Pilotrichella ampullaceae (Proctor 2002). The latter species can hold eight times as much water externally as internally (Proctor 2002). The external water has a water potential near zero and can evaporate fast without affecting the cell water balance (Zotz et al. 2000; Proctor 2004a). Intracellular water evaporates more slowly, but a strong evaporation barrier is lacking, so that all species eventually dry out if not remoistened. Still, if dense life forms grow in protected positions, e.g. in the forks of branches on accumulated humus, it may take days for them to dry out (Veneklaas et al. 1990).

High air humidity does not appear to activate carbon exchange in bryophytes (Lange 1969), although detectable fluorescence can be induced by air humidities above 95 % (Fig. 15.4 and M. Lakatos pers. com. 2011). For positive net photosynthesis relative humidity would probably have to be over 98 % (León-Vargas et al. 2006). The occurrence of such high humidity values could thus be a practical indicator of activity times in bryophytes.

Fig. 15.4.
figure 4

Resumption of chlorophyll fluorescence activity after dry bryophyte samples of two species (in equilibrium with RH 80 %, water content 15 % resp. 16 % of dry weight) were transferred into moist air (in jar above tap water), and cessation of activity after transfer back into drier air (RH 80 % in air-conditioned lab). Water contents in moist air rose to 49 % of dry weight in both samples. Dashed line: Zelometeoreum sp. Solid line: Orthostichopsis tetragona.

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Apart from environmental conditions and life forms, special morphological and anatomical structures that appear to affect water storage or water loss may also increase activity times of bryophytes (Biebl 1964). A general altitudinal trend in such adaptations can be recognized in the tropics, with water storage structures being more common in the lowlands, while water capturing structures are more common at high altitudes (Kürschner et al. 1999). Examples of water storage structures are enlarged hyaline cells in the leaves of common tropical mosses in the Calymperaceae and Leucobryaceae (Castaldo et al. 1979; Frahm 1997), and water lobules and water sacs (their size decreasing plastically with increasing humidity in some species) in leafy liverworts in the Frullaniaceae, Lejeunaceae and Radulaceae (Kürschner et al. 1999). Examples of structures reducing water loss are leaf-tip hairs and imbricated phylloids (Romero et al. 2006). Structures for water capturing (e.g. ‘fog stripping’), on the other hand involve increases in surface area, such as ciliate leaves, and usually present a trade-off with water storage.

C. Desiccation-Rehydration Frequency

When dry bryophytes are rehydrated, full recovery of photosynthetic rates can take up to several days, depending on the level of tolerance and the duration and intensity of the dry period (Proctor et al. 2007a). A higher cycling frequency has the advantage that no extended dry periods need to be survived (see section “Desiccation tolerance: desiccation duration and intensity” below), but it has several potential disadvantages for the carbon balance: direct carbon losses through resaturation respiration and carbohydrate leaching, reduced photosynthetic rates if recovery takes longer than the drying frequency, and an interference of repeated drying with this recovery (see also Chap. 9).

Immediately after rehydration, a so called ‘resaturation burst’ of respiration can be detected in gas-exchange measurements. A study on lichens in a lower montane rainforest revealed dark respiration rates four times higher than the steady state value 3 min after rehydration (Zotz et al. 1998). NP as well as Rd recovered to steady state values after 15–20 min. This high respiration is related to the restoration of membrane integrity and re-establishment of protein synthesis (Proctor 2000a, b); it may take from minutes to a day for photosynthesis to exceed respiration (Proctor 2002). Nutrients and carbohydrates may be lost at each rehydration event through leaching. Coxson et al. (1992) calculated that it would take fewer than 30 wetting/drying cycles to exhaust the internal sugar- and polyol pools of tropical montane bryophytes. The quantitative importance of resaturation respiration and leaching for the bryophyte’s carbon balance is largely unknown, but their influence would certainly increase with more frequent drying-wetting cycles.

Repeated cycles of hydration and dehydration caused greater loss of photosynthetic rates than continuous desiccation in Antarctic bryophytes from hydric habitats, while species from xeric habitats were better adapted to short periods of hydration (Davey 1997). For tropical species, we expect a similar relationship with continuous or highly intermittent moisture, but empirical evidence is lacking. The fastest hydration-rehydration cycles occur at exposed sites such as the outer canopy on days with intermittent precipitation. Such weather conditions are common in montane rainforests (see section “The physical setting”), occasionally allowing several cycles within a day (Norris 1990). Especially life forms with large surface areas, such as the pendant mosses so common in tropical montane forests, experience these rapid cycles and appear well adapted to this situation with fast recovery after rehydration (Zotz et al. 1997; Proctor 2002, 2004b).

D. Desiccation Tolerance: Desiccation Duration and Intensity

In non-seasonal rain- and cloud forests, bryophytes are hydrated nearly every day, so that species do not need adaptations to prolonged desiccation. Surprisingly then, Proctor (2002) found full recovery of two tropical pendant species even after 11 months of being stored dry (at 5 °C), which suggests a high degree of desiccation tolerance. Results of our own studies also indicate that desiccation tolerance is quite high in both lowland and lower montane rainforest species (>80 days for both, Bader et al. 2013). Even under changing precipitation regimes, desiccation tolerance as such is thus unlikely to limit future bryophyte distributions in the tropics.

Recovery from desiccation becomes slower and less complete as the desiccation period becomes longer, while recovery also depends on temperature and the intensity of desiccation (Proctor et al. 2007b). León-Vargas et al. (2006) measured compensation times, i.e. the time it takes for photosynthesis to compensate for respiratory carbon losses after rehydration, of Meteorium nigrescens, dry for 2–4 days. This species occurs either as a diffuse mass on palm trunks, or pendant on branches. The compensation time was nearly twice as long on the trunk (ca.100 min) as in the pendant form (60 min). This could be a form of acclimatization, as has been observed in colder ecosystems as well (Robinson et al. 2000), as the pendant experiences desiccation more often, for reasons already pointed out. Similarly, the pendant lower-montane moss Pilotrichella ampullacea showed compensation times of 30–60 min after 24 h dryness and 2–2.5 h after 6 days. This species recovered its Fv/Fm to normal values after 12 days of desiccation within ~40 h (Proctor 2002).

The intensity of desiccation, i.e. the water content of the desiccated moss, is generally not extreme in tropical rain forests, where relative air humidity rarely falls below 70 % (Biebl 1964, see section “The physical setting”). Bryophyte tolerances conform to these conditions: most epiphytic bryophytes studied (9/11) from a Puerto Rican montane forest did not survive 24 h at 52 % RH, 5/11 were damaged at 65 %, while most species from the forest floor (4/5) showed damage already at 75 % and some (2/5) even at 91 % (Biebl 1964). For comparison, bryophytes from xeric habitats can survive RHs <1 % (Höfler in Biebl 1962). The tolerance differences between species may also co-determine their local distribution within the forest.

Although desiccation damage generally increases with desiccation intensity (Biebl 1964; Proctor 2004b), mild desiccation can sometimes impose more damage than deep desiccation, especially in xeric species (Proctor 2001). Under mildly dry conditions some physiological processes, such as respiration, do not cease completely and can cause metabolic imbalances, while pathogens may provoke further damage (Proctor 2001; Proctor et al. 2007b). Due to the constantly high air humidity, bryophytes in tropical rainforests are exposed to mild desiccation only.

V. Effects of Light and CO2 on Carbon Balance

Light conditions vary widely among bryophyte habitats, also in the tropics (see section “The physical setting”). Overall, the observed light responses of tropical mosses and hepatics are in the range of those observed at other latitudes (Larcher 2001). Published light compensation points (LCPs) range from 5 μmol m−2 s−1 in Pilotrichella flexilis to 35 μmol m−2 s−1 in Macromitrium cirrosum (Table 15.2). As expected, the lowest LCPs are exhibited by bryophytes from the forest floor where irradiation is lowest or in the inner crowns of trees. Highest LCPs are found in bryophytes growing on exposed branches or on logs where irradiance is high at least during parts of the day. Although photosynthesis saturates at rather low PFD (200–400 μmol m−2 s−1; see Proctor 1982, 2004b; Zotz et al. 1997) light is limiting for bryophytes and lichens for most of the day even in the forest canopy (for comparison see Zotz and Winter 1994). The extremely high PFD levels reported in section “The physical setting” have little relevance for photosynthesis: light becomes limiting for photosynthesis especially during and after rain events, when bryophytes and lichens are wet and could potentially achieve high photosynthetic rates (Lange et al. 2004).

Light compensation points can shift to lower light levels if CO2 levels are increased (Silvola 1985), although long-term effects of higher CO2 tend to decrease through acclimatization (Tuba et al. 2011). Actual rates of photosynthesis increase with increasing CO2 concentrations, and CO2 concentrations in a bryophyte’s microhabitat can be more than 100 ppm over concentrations in ambient air (Tarnawski et al. 1992, 1994; Pannewitz et al. 2005 and see section “The physical setting”). There is no information available of CO2 responses for tropical bryophytes or lichens in particular. However, for bryophytes in general effects of elevated CO2 can be substantial (Tuba et al. 1999, 2011). For example, Silvola (1990) reports that Sphagnum fuscum increases photosynthetic rates by 30–50 % when CO2 concentration is raised from 300 to 500 ppm.

VI. Effects of Temperature on Carbon Balance

In all plants, the temperature response of photosynthesis typically follows an optimum curve, while dark respiration increases exponentially with increasing temperature (e.g. Lange 1980; Proctor 1982; Atkin and Tjoelker 2003). Temperature may affect respiration more strongly in colder climates like the Arctic (Q10 = 2.6) than in warmer environments like the tropics (Q10 = 2.1) (Atkin et al. 2005). As shown above, photosynthetic carbon gain in non-vascular plants is limited by various factors. Temperature-effects on photosynthesis rates are probably relatively unimportant in limiting carbon gain, but carbon loss due to high respiration rates at high night temperatures may pose a problem for tropical lowland bryophytes (Richards 1984). Surprisingly though, a recent study found no differences in the ratio of dark respiration to net photosynthesis rates between montane and lowland species under the respective temperature conditions at the altitudes of origin (Wagner et al. 2013). Higher temperatures may thus affect carbon balance more by increasing evaporation rates, i.e. by decreasing activity times, than by direct effects on metabolic rates.

Temperature optima for photosynthesis in arctic and temperate bryophytes generally range between 5 and 20 °C, though optima up to 24–30 °C have been reported even for Arctic species (summarized in Frahm 1990b; Larcher 2001). For tropical lowland and lower-montane bryophytes from Panama, temperature optima closely matched local temperature conditions, with optima shifting from ca. 26 to 20 °C between 0 and 1,200 m (Wagner et al. 2013). In contrast, the optimum temperature for the lowland lichen Parmotrema endosulphureum (Zotz et al. 2003) was rather low at 22 °C and similar to that of the montane lichens Dictyonema glabratum (Lange et al. 1994) and Pseudocyphellaria aurata (Lange et al. 2004), suggesting no special adaptation to high temperatures. Frahm (1990b) found optimum temperatures of 15 °C for a montane rainforest species (from 2,300 m) under high light conditions. He simulated lowland and highland temperatures with two different light levels. Consistent with Richards’ (1984) notion, highland conditions (15 °C, 1,500 Lux) were associated with positive carbon balances for the investigated species, while under lowland conditions (30 °C, 300 Lux) respiration exceeded gross photosynthesis even during light periods (Frahm 1987b, 1990b). However, it is not unlikely that these results are related to ex-situ cultivating, which is rather difficult with tropical species (M.Y. Bader et al. personal observation).

The results of a single study are at odds with Richards’ hypothesis (Lösch et al. 1994). This laboratory experiment with upper-montane bryophytes from Africa using Warburg manometry showed only a small effect of dark respiration on CO2-exchange under lowland conditions. Temperature responses differed little between species from 800 and 3,200 m. Again, this surprising result could be an artifact of the high CO2 concentrations supplied in the method used, or is similarly related to the fact that all species had been cultivated at the same temperature for 2 months before the measurements. In any case, these methodological concerns do not allow unambiguous conclusions.

A. Temperature Acclimation

A likely response to higher temperatures is metabolic acclimatization. Many vascular plants can down-regulate their dark respiration to acclimatize to a prolonged increase in temperature, but differences in this acclimatization potential between plant groups and climate zones are incompletely understood (Atkin et al. 2005). Seasonal acclimatization has been documented for temperate and polar bryophytes (Longton 1988). For example, Hicklenton and Oechel (1976) observed an acclimation of temperature optima after 72–120 h in experiments with Dicranum fuscens. In polar ecosystems, optimum-temperatures for bryophyte photosynthesis are seasonably variable, with optima varying up to 10 °C even within the summer season (Skre and Oechel 1981). However, tropical bryophytes normally experience much smaller changes in temperature and therefore their acclimatization potential might be smaller.

This acclimatization potential is of critical importance both for the question of the physiological basis of current altitudinal distribution patterns and for the likely responses of bryophytes to climate change. We quantified this potential in a transplant experiment by transporting cut branches covered with different bryophyte species from a lower montane rainforest (1,200 m) to sea level (Fig. 15.5). With acclimation we would expect a reduction of dark respiration after transplantation, but during the 16 days of the experiment no such acclimation was observed (means within or below confidence intervals at t = 0), while samples suffered obvious damage. Although suggesting a lack of acclimatization, this experiment cannot provide conclusive answers yet: longer-term monitoring, shorter transplantation distances (i.e. smaller temperature differences and lower stress levels) and larger sample sizes are necessary for stronger conclusions about the acclimatization potential of tropical bryophytes.

Fig. 15.5.
figure 5

Change of net photosynthesis (open symbols) and dark respiration (filled symbols) of three lower-montane bryophyte species (from Fortuna, ca. 1,100 m, Panama, see section “The physical setting”, S. Rottenberger and G. Zotz unpublished data) after transplantation to the lowlands (at t = 0, first measurements were made directly after transplantation). Gas exchange rates were measured at optimum water content, cuvette temperature of 25 °C and PFD 600 μmol m−2 s−1 (photosynthesis) or in the dark (respiration). Values are means of 3–4 moss canopies, error bars indicate 95 % confidence intervals; the dotted/dashed lines continue the confidence intervals at t = 0. The lowering of net photosynthesis in Toloxis imponderosa and Phyllogonium viscosum probably indicates a general decline in health; all species showed clear evidence of damage after 2 weeks.

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VII. Nutrients

Nutrient requirements in bryophytes are similar to those of vascular plants (Shaw and Goffinet 2000; Waite and Sack 2011a). So far we have discussed reasons why tropical epiphytes may be carbon limited, but nutrients could be limiting growth as well, although in situ growth does not appear to be nutrient limited in most mosses and liverworts (Oechel and Sveinbjörnsson 1978). In the tropics, where bryophytes mostly occur as epiphytes, the situation may be very different from arctic and terrestrial systems, where most studies have been carried out (Oechel and Sveinbjörnsson 1978; Jauhiainen et al. 1998). A single study addresses nutrient limitation for bryophytes (and lichens) in a tropical system. Abundance and species richness of non-vascular epiphyte communities in Hawaii increased dramatically after experimental P (but not N) addition to the forest soil (Benner et al. 2007). Especially N-fixing cyanolichens profited, suggesting that at least these were P-limited before fertilization. Phosphorus is also commonly the most limiting nutrient for vascular epiphytes, although water is nearly always more limiting (Zotz 2004). In some cases this may be true also for non-vascular epiphytes (Benner et al. 2007), which also rely mainly on aerial nutrient sources (Clark et al. 1998, 2005; Tozer et al. 2005; Chen et al. 2010), though nutrients leached from the host tree or from decomposing plant parts can also be used (Goward and Arsenault 2000; Hietz et al. 2002). There is no indication, however, that nutrient inputs follow consistent altitudinal patterns around the tropics. So although tropical bryophytes are understudied in relation to nutrients, the major distributional patterns discussed in this review are hardly caused by differences in nutrient supply.

VIII. The Fate of Non-vascular Epiphytes under Global Change

Accepting the notion that tropical lowlands are already marginal habitats for bryophytes (and lichens) today due to high temperatures, the predicted increase of 2–5 °C for the tropics in the next 100 years (Solomon et al. 2007) may be particularly critical for this plant group. Climate change will certainly cause changes in species composition in general but the likelihood of extinction is difficult to predict unless fundamental temperature or moisture tolerances are exceeded (Wright et al. 2009). This may indeed be the case for bryophytes as a group.

In order to estimate the threat of the tropical lowlands becoming virtually devoid of bryophytes in the future, one approach is to model bryophyte carbon balances based on measured response curves and including potential losses through leaching and repair after desiccation. Such a model would allow us to identify the driving factors influencing bryophyte carbon balance in general and developments in the tropics under different climate change scenarios, in particular. Based on carbon exchange data and using a very simple model, Zotz and Bader (2009) estimated the theoretical carbon balance of the lowland lichen Parmotrema endosulphureum under climatic warming. With a temperature rise of 3 °C this lichen would have to increase its daily activity (at optimal rates) from 40 % of the light period to over 90 %, which is virtually impossible under tropical conditions. However, this model still needs refining and it needs actual data for tropical bryophytes in order to allow any predictions for this group.

Another approach to look into a warmer future is the experimental warming of existing species and communities. This can be achieved through transplantation to lower altitudes (Nadkarni and Solano 2002; Jácome et al. 2011), or through experimental warming in situ, though this has never been done for epiphytic mosses. We are currently initiating such a study which will pay particular emphasis to the interactive effects of temperature and CO2.

Poikilohydric organisms like bryophytes and lichens could be threatened not only by a future warming but also by changes in precipitation regimes (Zotz and Bader 2009). Increased drought frequency, as reported for Amazonia recently (Lewis et al. 2011), might negatively affect non-vascular epiphytes. Although drought tolerance far exceeds the currently longest local droughts in a variety of both montane and lowland bryophyte species (Proctor 2002; Bader et al. 2013), tolerances are certainly species-specific. Community compositions may thus be altered, even if communities do not collapse altogether (Hughes 2000), as was found in a transplantation experiment of montane bryophytes to a warmer and drier altitude (Jácome et al. 2011). By altered species composition or directly through effects of altered hydration regimes on the carbon balance, biomass and ecosystem functioning may also be affected by precipitation changes.

IX. Conclusions

The strong altitudinal gradient of bryophytes in the tropics is much-discussed but a so far little-studied phenomenon. Hypotheses explaining the paucity of bryophytes in the lowlands also have direct implications for the responses of tropical bryophytes to climatic changes and thus merit attention not only in the light of scientific curiosity.

Promising approaches for investigating these hypotheses include modeling of carbon balances, based on real input data (which thus need to be collected!) such as carbon-exchange responses to temperature, light, moisture, CO2, as well as good estimates of these abiotic factors at the bryophytes’ growing sites. Another approach is the experimental manipulation of hypothesized environmental influences. The most obvious candidate, of course, is temperature, while interesting interactions can also be expected with moisture and CO2.

In conclusion, based on current knowledge it is likely, though as yet not unambiguously shown, that the globally observed altitudinal distribution patterns of tropical bryophytes have a rather simple physiological basis. We can exclude, though, that differences in drought tolerance play a major role in shaping these patterns. The delicate balance between carbon uptake and loss and the important role of temperature and precipitation regimes in determining this balance imply that predicted changes in global climate may have dramatic effects on bryophytes and lichens in the moist tropics.