Some Results of 2 Years' Data Logging on Grimmia Pulvinata

How long must a desiccation-tolerant moss tolerate desiccation? Some results of 2 years’ data logging on Grimmia pulvinata

Michael C. F. Proctor

Department of Biological Sciences, University of Exeter, Washington Singer Laboratories, Perry Road, Exeter, Devon. EX4 4QG, UK E-mail: [email protected] Received 17 December 2003; revised 24 February 2004

Grimmia pulvinata (Hedw.) Sm. is a common desiccation- average factor of 1.7, and the number of dry–wet cycles less tolerant moss of wall tops in Britain. Readings were recorded at than the number of precipitation events by a factor of 3 or 30-min intervals from sensors measuring duration of precipita- more, especially during autumn and winter. There was little tion, ‘moss wet’, solar irradiance, net radiation, air temperature indication of hydration following dew-fall. The proportion of and moss temperature. The duration of both ‘moss-dry’ and the time the moss was wet in daylight at any time of year was ‘moss-wet’ periods varied widely, but generally approximated nearly proportional to the fraction of the 24 h between sunrise to a log-normal frequency distribution. The median length of and sunset. Most growth took place in autumn and early winter dry and wet periods was relatively short, generally between 5 when (with relatively low irradiance) the moss was wet for long and 15 h. The longest dry periods, recorded in early summer, periods and the weather was still mild. Desiccation-tolerant were 15 and 17 days, and the longest continuously wet period bryophytes (and lichens) are pre-eminently organisms adapted (almost 28 d), in the unusually wet autumn of 1988. The moss to frequent, and often short, dry–wet cycles. This should be a was generally wet for longer than the duration of rain by an prime focus of research on their physiology.

Introduction Bryophytes are well known for their desiccation toler- in approaching some of these questions, and their ance, and there is abundant experimental evidence that physiological implications for desiccation-tolerant bryo- many will survive and recover after drying to very low phytes, this paper presents some results of 2 years’ data water content for weeks, months or even years (Maheu logging on Grimmia pulvinata (Hedw.) Sm., a small 1922, Abel 1956, Hosokawa and Kubota 1957, Keever desiccation-tolerant cushion-forming moss, common on 1957, Dilks and Proctor 1974). However, there is little walls in Britain and neighbouring parts of continental information on the length of the dry and wet periods that Europe. bryophytes actually experience in the field. Twenty-two ‘rainless’ periods ranging in length from 37 to 73 days were recorded in the British Isles from the 1890s to the Materials and methods 1990s (Dukes and Ede 1997), but this defined as ‘rainless’ a day with 0.2 mm of measurable precipitation, so The measurements were made on a population of Grimmia many of these dry periods were probably not truly rain- pulvinata on a mortared hard sandstone garden wall less. Further, really long dry periods are clearly rare, and about 1.7 m high near Morchard Bishop in mid-Devon, most dry periods in the British climate must be very south-west England (Lat. 50510 N, Long. 3450 W; much shorter. Dry periods will tend on average to be OSGB ref. SS 773 066), 145 m above sea level. Mean shorter in high-rainfall oceanic climates, and longer monthly temperature in January is approximately 4C, in climates that are more arid and more seasonal, as in and in July approximately 15C. Average annual rainfall the Mediterranean and subtropics. As a starting point is approximately 1000 mm; monthly rainfall during the

Abbreviations – OSGB, Ordnance Survey of Great Britain.

Physiol. Plant. 122, 2004 21 observation period at Kennerleigh, approximately 5 km with repeated short showers the factor may sometimes be east of the recording site and at slightly lower altitude, much greater than this, and occasionally light but detect- is shown in Fig. 1. able rainfall failed to moisten the moss at all, the rain- The equipment consisted of two Grant ‘Squirrel’ drops remaining poised on the hair-points at the tips of recorders (Grant Instruments, Shepreth, Cambs., UK). the leaves. Only rarely was there any indication of hydration One recorded moss temperature and air temperature (in following dew-fall, probably partly because the wall a well-ventilated, cylindrical, bright-metal radiation was an effective heat store or sink, and partly because of screen) from thermistors. The other recorded mV out- relatively free convective heat exchange with the air. The puts from a tube solarimeter and a tube net radiometer ‘duration of precipitation’ measured was always substan- (Type TRM; Delta-T Devices Ltd, Burwell, Cambs., tially greater than that indicated by the Meteorological UK), and from two resistance probes (made from a Office figures for duration of rainfall (about 800 h per pair of platinum wires tightly wound figure-of-eight- year, or approximately 10% of the time for this site), wise with polyester thread and sealed at the ends with which refer to ‘measurable’ rainfall. epoxy resin), approximately 1 cm long, connected to a The data also show clearly that the frequency of dry– simple resistor network powered by a 1.5-V battery to wet cycles was in general less (by a median factor of give an output between 0.4 mV (dry) and 11.4 mV 3.29), and often much less, than the frequency of discrete (saturated). One of these probes was half-immersed ‘precipitation events’ recorded (Fig. 3). The effect was across the surface of a Grimmia cushion (measuring very much more pronounced in autumn and winter ‘moss wet’), and the other was freely exposed to the air than in spring and summer; apart from one peak in (measuring ‘duration of precipitation’). The threshold August the highest quotients are all in the winter half value between ‘dry’ and ‘wet’ was arbitrarily taken as of the year between September and March (Fig. 3B). The 0.0 mV for both probes. Because the resistance ranges so monthly number of dry–wet cycles showed a well marked widely between wet and dry conditions the output concentration in the spring and early summer months, approximates to an all-or-nothing curve, and the exact with the exception of May 1989 in which very little rain threshold value chosen makes little difference to the fell at all. results. Readings were recorded at 30-min intervals The foregoing results leave aside the length of individ- from early May 1988 to April 1990. The record is essen- ual dry and wet periods. Plotting the measured length of tially continuous over this period, with only a few gaps wet and dry periods as cumulative frequencies showed a of up to about a week, mostly due to equipment mal- fair approximation to a set of cumulative normal distri- functions. bution curves on a logarithmic time scale. This is illus- trated by the data for the 3 months from June to August Results 1988 in Fig. 4. For description and comparison the cumulative frequency plots are usefully fitted by sigmoid The measurements show that, as would be expected, the logistic curves. These give a good fit to most of the data moss remained wet for substantially longer than the time sets, except for the winter wet-period measurements, precipitation was actually falling (Fig. 2A); capillary where 3 months is probably too short a time to sample water storage in the moss cushion generally increased potential long wet periods adequately, and there is a the time the moss was hydrated by a factor of about similar tendency to truncate the curves for dry periods 1.7. However, as shown in Fig. 2B, in unsettled periods in late summer (Fig. 5). However, these curves show very

Fig. 1. Monthly rainfall at Kennerleigh, Devon, UK (Lat. 50510 N, Long. 3410 W; OSGB ref. SS 819 074, alt. 120 m), approximately 5 km E of the measurement site, during the period of observation. Rainfall at Lapford, approximately 5 km W of the measurement site was closely similar.

22 Physiol. Plant. 122, 2004 Fig. 2. A, Percentage of time with precipitation (.) and percentage of time moss wet (*) in arbitrary recording periods (generally 5–8 days). Note that the recorded ‘time with precipitation’ will depend on the sensitivity of the sensor, and is inherently not sharply bounded. B, Quotient of ‘time moss wet’ and ‘time with precipitation’.

clearly the shift in the relative lengths of wet and dry that the moss was dry for substantial periods at all periods through the seasons, and the tendency of the times of year. curves for both dry and wet periods to flatten with As Fig. 7 shows, the proportion of time the moss was increasing average time dry or wet. The period of obser- wet in daylight at any time of year was roughly propor- vation happened to embrace a particularly dry summer tional to the fraction of the 24 h between sunrise and and an exceptionally wet autumn and winter; the data sunset. It was depressed only slightly by higher tempera- for the driest and wettest 3 months show the seasonal ture and greater net radiation income in summer, and the contrast close to its most extreme (Fig. 6). longer daylight hours at that season more than compen- Themedianlengthofbothdryandwetperiodsat sated for this. all seasons was notably short – in most cases between The radiation and temperature measurements will not be 5 and 15 h, the single exception being the 25 h median considered further in this paper; however, it may be noted dry period in late summer 1989 (Table 1). The longest that moss temperature generally remained within 10Cof dry periods recorded were about 17 days in summer air temperature (and below 35C) as long as the moss was 1988 and 15 days in summer 1989. The longest wet, but temperature differentials of 20Cormore(with continuously wet period (almost 28 d) was recorded surface temperatures exceeding 45C) could develop in hot in the unusually wet autumn of 1989. It is noteworthy sunny summer weather when the moss was dry.

Physiol. Plant. 122, 2004 23 Fig. 3. A, Daily mean frequency of precipitation events (.) and moss dry–wet cycles (*) in arbitrary recording periods (generally 5–8 days). Note that the number of ‘precipitation events’ recorded depends on the threshold assumed between ‘wet’ and ‘dry’, so is sensor-dependent. B, Quotient of precipitation events and moss dry–wet cycles.

Discussion support bryophyte growth at all will have a pattern of The maximum length of dry periods recorded is well individual wet and dry spells. Vascular plants experience within the known tolerance of many desiccation-tolerant varying degrees of water stress in the soil. Ectohydric bryophytes. Even the longest ‘rainless’ periods of the bryophytes are in general either wet (and fully turgid) meteorological statistics would not seriously challenge or dry (and metabolically inactive). For them, all habitats the more tolerant species (Proctor 2001, 2003). What are ‘mesic’ when it has rained, and all habitats are ‘arid’ may perhaps come as a greater surprise to habitual pat- when it has not. ‘Water stress’ in the usual sense is a terns of thought is the high frequency of short dry per- relatively brief transient state between periods at full turgor iods, and also of short wet periods. This implies that we and periods of desiccation. From the point of view of a should give much more attention to the physiological desiccation-tolerant bryophyte or lichen, the difference responses of bryophytes to frequent shifts between between mesic and arid habitats lies in the relative length short dry and wet periods, and that this may often of time spent wet and dry, not in any measure of water more relevant to the day-to-day survival of desiccation- stress appropriate to ‘homoihydric’ vascular plants tolerant bryophytes than their tolerance of prolonged (Proctor 2000, Proctor and Tuba 2002). periods of desiccation. The present results are of course from a single site, in one year in one particular climate. Wet and dry periods and moss growth Results in other places will obviously be quantitatively different, but qualitatively are likely to follow a similar Recovery of net photosynthesis from even short periods broad pattern. Even the wettest climate has dry periods, dry is not instantaneous (Tuba et al. 1996, Proctor and and any climate with regular-enough seasonal rain to Pence 2002); some 10–20 min must elapse before net

24 Physiol. Plant. 122, 2004 Fig. 4. Cumulative frequency plots of the lengths of ‘moss-dry’ and ‘moss-wet’ periods, June–August 1988, with fitted logistic curves. Time-resolution at the lower end of the curves is constrained by the 30-min sampling interval of the recorder, so the numerous readings at 0.5 h include a proportion of dry or wet periods which were in fact shorter or somewhat longer. In the corresponding plots for January– March 1989, the data for dry periods give a fair approximation to a logistic curve with asymptote 1.0. However, the data for wet periods show no clear sign of an asymptote, probably because the 3-month sampling period is too short for adequate sampling of long wet periods, thus truncating the distribution; the mid-point value of the fitted logistic curve suggests a wet-period modal length of approximately 27 h (see Table 1).

photosynthesis becomes positive, and 30 min or an being able to cope with frequent changes from dry to hour may be needed to restore the carbon balance of wet – from an anhydrobiotic state to fully active meta- the moss over the whole dry–wet cycle. From this con- bolism – and back again, often within an hour or less. sideration alone, little growth would be expected in the Grimmia pulvinata, growing on exposed rock surfaces spring and early summer months with half the wet may be near one end of a spectrum from ‘high-inertia’ periods less than 6.5 h, and three-quarters less than 17 to ‘low-inertia’ desiccation-tolerant plants (Tuba et al. h. Throughout the year, wet periods of less than approxi- 1998, Proctor and Tuba 2002), but with the water- mately 2 h were frequent, a substantial proportion of storage provided by its dense cushion habit (Zotz et al. these certainly being short enough to lead to a net carbon 2000) it is by no means an extreme case. Such bryophytes loss. However, in autumn and winter these were offset as Frullania dilatata on rock surfaces and Tortula by the predominance of very much longer wet periods, (Syntrichia) ruralis on rooftops or in dry grassland, and and generally fewer dry–wet cycles. It is in the autumn saxicolous crustose lichens such as Rhizocarpon geo- and early winter, characterized by long wet periods, low graphicum, probably switch states more frequently than radiation income and relatively mild temperatures that the Grimmia. All must retain their essential metabolic most growth took place (Proctor and Smith 1995). systems through a dry–wet cycle in a state from which The present results underline the fundamental import- they can quickly be reactivated. This contrasts with ance to desiccation-tolerant bryophytes and lichens of many angiosperm ‘resurrection plants’, in which there

Physiol. Plant. 122, 2004 25 Fig. 6. A near-extreme case: cumulative frequency curves for the driest and wettest 3-month periods during the period of observation. A, May–July 1989; B, December 1989–February 1990. Fig. 5. Fitted cumulative frequency curves for moss-dry and moss- wet periods during successive 3-month intervals in 1989. In the upper diagram (A), note the progressive rightward shift of the curves, towards longer dry periods, from winter to late summer, and may be time for significant metabolic changes enhan- the reverse of this trend in autumn. The wet-period curves (B) show cing tolerance as the plant dries out, and extensive a general tendency to shift to the left and steepen in spring and early summer, and to flatten in autumn and winter with the increasing repair processes on rehydration (Hartung et al. 1998, frequency of long wet periods. Note that dry periods, and short wet Kappen and Valladares 1999, Black and Pritchard 2002, periods, occur at all times of year. Proctor and Tuba 2002). Desiccation-tolerant bryophytes and lichens should thus be seen as organisms

Table 1. Grimmia pulvinata. Length of moss-wet and moss-dry intervals recorded at Morchard Bishop, Devon, UK, during 1989: descriptive parameters (hours). The logistic fit tends to be truncated at its upper end for wet periods in winter and for dry periods in summer; its mid-point (representing the steepest point on the fitted curve and the mode of the fitted distribution) is then substantially greater than the (non- parametric) median value of the raw data.

Time interval Quartile 1 Median Quartile 3 Maximum Mid-point of logistic fit Dry Jan–March 1989 1.75 5.5 12 123.5 4.76 Apr–June 1989 2.25 5.5 29.125 367.0 7.30 Jul–Sept 1989 6.5 25 104.5 255.0 52.94 Oct–Dec 1989 2.75 9.75 27.125 267.5 9.48 Wet Jan–March 1989 2.125 14.5 37.25 161 26.59 Apr–June 1989 1.5 6.5 17.0 72.0 13.83 Jul–Sept 1989 1.5 10.0 17.5 152.5 10.91 Oct–Dec 1989 0.875 11.0 103.75 669.0 17.66

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Edited by M. J. Oliver

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