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Diurnal migration and responses to simulated rainfall in desert soil microarthropods and nematodes
Sorl Bwl 8,o‘lw”l Pnntcd in Great
voi 13. pp 417 to 425. 1981 Br,tam All right,, reserved
Copynght
0038-0717.‘b1.050417-09SO2.00~0 0 1981 Pergamon Press Ltd
DIURNAL MIGRATION AND RESPONSES TO SIMULATED RAINFALL IN DESERT SOIL MICROARTHROPODS AND NEMATODES WALTER G. WHITFORD, DIANA W. FRECKMAN’, NED Z. ELKINS, LAWRENCE W. PARKER, ROB PARMALEE’,JANICE PHILLIPS
and SUZANNE TUCKER Department of Biology, New Mexico State University, and ‘Department
of Nematology,
University
(Accepted
Las Cruces, NM 88003, U.S.A. of California, Riverside, CA 92521, U.S.A.
10 February
1981)
Summary-Diurnal
patterns of microarthropod abundance in surface leaf litter were related to its moisture content. Leaf litter moisture was nearly 7% by weight at 0800 h but fell to less than 1% by mid-day. Oribatid and tydeid mites moved into litter in the early morning and back into the soil before mid-day. There were no significant differences in numbers of nematodes in litter or soil and 78%98% of the nematodes were anhydrobiotic (coiled) in soil and litter at all times sampled. Following simulated rainfall there were fewer microarthropods in litter at mid-day in the absence of marked decreases in soil and litter moisture content. During drying, there were gradual reductions in numbers and species diversity of litter microarthropods. Nematode numbers did not change as litter dried. Anhydrobiotic nematodes in the soil increased from 14% on day 1 to 85% on day 4. Between 24 and 36 h after simulated rainfall, the proportion of anhydrobiotic litter nematodes increased from 35 to SO”l,,. Within I h after simulated rainfall, there were marked increases in numbers and diversity of microarthropods in surface litter. No collembolans were extracted from dry litter controls but the wet litter was dominated by isotomid, sminthurid and onychiurid collembolans. There were increases in numbers and diversity of oribatid, tydeid and gamasid mites in the wet surface litter within 1 h after wetting compared to controls.
INTRODUCTION Most desert ecosystem processes are regulated by rainfall (Noy-Meir, 1973, 1974). The frequency, amount and seasonal occurrences of rain, undoubtedly have varying effects on productivity, decomposition, population dynamics and behavior of the biota. The effect of rainfall on a process is dependent upon the time that process takes to respond. Because of the short time needed to initiate population growth of microorganisms, or to activate the microfauna, decomposition processes should exhibit rapid responses to wetting and drying. Few of these responses have been examined in desert ecosystems. Wetting and drying affects decomposition, microbial respiration and mineralization (Birch, 1958, 1964; McGregor, 1972). Little attention has been given to the dynamics of the soil biota during cycles following rainfall (Metz, 1971). In Chihuahuan desert ecosystems, organic matter is distributed in patches and the density and diversity of soil microarthropods varies as a function of litter quantity (Santos et al., 1978). Numbers of free-living nematodes are also higher in areas of litter accumulation under plants (Freckman and Mankau, 1977). As soon as the littersoil systems becomes rapidly and nitrogen
wet, organic is mineralized
matter decomposes (Birch, 1958, 1964)
1976) and may be activated by an increase in available moisture. Acarina may migrate from the moister environment of the mineral soil to litter (Metz, 1971). Prot and Netcher (1978) showed that Meloidogyne larvae in soil migrated 45 cm in 10 days to tomato roots suggesting that nematodes may undergo vertical migration in agricultural soils. Thus, the soil microfauna could respond to rainfall by vertical movements or activation from the anhydrobiotic state. Another process in desert litter-soil systems which may affect the behavior of the soil fauna is the movement and condensation of water vapor in the soil which results from diurnal heating and cooling. Because of the different thermal characteristics of litter with respect to soil, it is possible that water vapor which has moved up through the soil during the day may condense on the surfaces of leaves in the leaf litter at night. Thus, even in dry soil, diurnal differences in temperature or moisture could affect the behavior of the soil fauna. We report experiments designed to examine the behavior of a desert soil fauna in response to simulated rainfall. We also examined diurnal changes in soil and litter fauna in unwatered soil-litter systems. METHODS
suggesting a number of potential activities of the soil fauna. Some soil fauna (nematodes, tardigrades and collembola) are capable of anhydrobiosis (remaining alive in a dehydrated state with unmeasurably low metabolism) (Demeure et al., 1979; Poinsot-Balaguer,
Most of the studies were done on a site 13 km east of Las Cruces, New Mexico on a nearly flat peneplain of rocky, sandy-loam soil and sparse vegetation cover of creosotebush, Larrea tridentata (Cov.). Studies of 411
418
G.
WALTER
WHITFORD et al samples which were placed in modified Tullgren funnels to extract microarthropods. Nematodes were extracted from the remaining three litter and soil samples (see below). In the simulated rainfall experiments, 96 screen cylinders received the equivalent of 25.4 mm water. The wetting front in the soil below the litter expanded to an 18 cm circle. At 0400, 1400 and 2200 h, and on days 1, 2, 4 and 8 following the simulated rainfall, 8 cylinders were collected. Each sample consisted of the litter from the cylinder and a soil sample to 6 cm below the wet litter. Microarthropods were extracted from three samples and nematodes from the remaining five. Soil and litter temperatures were measured with a standard laboratory thermometer. Temperatures at the soil litter interface were recorded by carefully sliding the bulb under the litter along the soil surface until the bulb was covered. Soil temperatures were
immediate response to wetting were done 3 km east of Las Cruces, New Mexico on a site with deep sandy soil bearing a mixture of creosotebush and mesquite. Prosopis glandu/osa (Torr.). Litter was collected from under creosotebushes. The litter was approximately 60”/, creosotebush leaves with the remaining 407, annual plant parts, rabbit feces, mesquite leaves and parts of grasses. Twenty grams of litter for nematodes and 25 g of litter for other measurements was confined in open-bottom screen cylinders (9.8 cm dia) to prevent litter from being scattered. These quantities approximate the concentrations of litter normally found under shrubs in the area. The litter in the cylinders was left in the field for 6 days before simulated rainfall. Forty-eight cylinders were not given simulated rainfall. Six collections of these were made throughout 24 h at 0100, 0400, 0800, 1400, 1800 and 2200 h. Each collection consisted of five litter and five soil
.
SOIL-LITTER
INTERFACE
n MOISTURE
TEMPERATURE
BY WEIGHT
8
\
oI
I
I
2
I,
I,
4
‘I
6
I
6
I
10
I1
I
12
/-
‘m’ I
14
I
I
16
I
I
16
I
I
20
I,
I
22
24
HOURS
Fig. 1. Diurnal changes in numbers of microarthropods and nematodes extracted from soil and litter in relation to mean soil-litter interface temperature and mean litter moisture. The black bars below the time scale indicate periods of darkness, The top panel summarizes the data for nematodes with the height of the bar equalling the mean and the lines equalling & 1 SD. The middle panel summarizes the data for microarthropods with the height of the bar equalling the mean and the lines equalling + 1 SD.
Behavior
of desert soil microfauna
419
p NANORCHESTIOS IID OTHER MITES
0
0100
0400
1400
0600
1600
2200
HOUR
Fig. 2. Comparison
of mean numbers of different samples collected
by inserting the thermometer into the side of the bottom of the hole left when soil samples were removed. The samples for microarthropod extraction were collected into “ziplock” plastic bags, returned to the laboratory; microarthropods extracted in modified Tullgren funnels into water (Santos et al., 1978) and then counted. Subsamples were removed from these 25 g samples for litter moisture content and to estimate bacterial and protozoan numbers. Soil and litter moisture was determined by the gravimetric method (105°C for 24 h). Estimates of bacterial and protozoan numbers were made from the 1400 h samples on days 1 and 4 only. Bacterial numbers were estimated by direct counts using the FITC staining technique (Babiuk and Paul, 1970). Total and cystic protozoa were counted by the most-probable-number method (Singh, 1946). Cyst numbers were obtained by soaking 2g plant material in 2% HCl for 24 h at room temperature, the acid was neutralized and protozoan trophs were estimated as the difference between the total counts and cyst numbers. Nematode soil samples were taken beneath the litter with 7.5 cm dia oak field tube. Three samples each of litter and soil were mixed into containers of 5% formalin for later extraction of coiled and straight nematodes by the anhydrobiotic extraction technique (Freckman et a/., 1977). Two additional samples from both soil and litter were immediately placed in water for 12 h to obtain active, rehydrated nematodes, then preserved in 5% formalin for identification. Nematodes were extracted from litter and soil by a modified sugar floatation technique (Freckman et al., 1975) taken
taxa of microarthropods at the times indicated.
extracted
from litter and soil
but, most nematodes were unidentifiable due to in cico preservation in soil combined with the extraction technique. Initial results indicated that considerable activity developed immediately following a rain. In another set of experiments, the microarthropod fauna in litter and soil were compared l-8 h after wetting. We used 30 g litter moistened with the equivalent of 25.4 mm rainfall. Five replicates of each wet litter, dry litter, and upper 8 cm of soil under the litter were immediately returned to the laboratory and extracted. RESULTS
The diurnal movements of microarthropods into the surface litter was related to litter moisture and the litter-soil interface temperature (Fig. 1). Litter moisture reached nearly 7”/:, at 0800 h but fell rapidly to less than 1% by mid-day. There were significantly fewer microarthropods in the litter at 0400 and 1800 h (F = 15.8, P < 0.01). However, in the soil, the only significant reduction in numbers was at 2200 h (F = 5.38, P < 0.01). There was a significantly higher litter moisture at 0800 h than during the night (F = 15.8, P < 0.01). Some groups of Acarina moved from soil to litter and back into the soil. (Fig. 2). Oribatids moved into the litter in the early morning when temperatures at the soil litter interface were moderate and litter moisture was greater than 5% (Figs 1 and 2). Tydeid mites were in the litter when temperatures were moderate but apparently moved into the deeper soil at high temperatures. Tarsonemid mites (X = 3 per 25 g) were found only in litter samples from 0400 h. lsotomid
WALTERG. WHITFORDet al.
420
Table 1. Litter and soil moisture at 6cm (expressed as percent by weight); wet and dry soil temperatures following water amendment equivalent to 25.4mm. The percent moisture of the dry soil during the experiment was 0.55 + 0.01. On day 7 there was a natural rainfall of 25 mm at 1630 h Temperature Wetted soil
( C) Dry soil
Litter
Soil
Day 1 04OOh 1400h 2200 h
16.0 k 2.6 8.7 * 3.0 5.7 + 1.7
8.7 f 3.1 4.0 f 2.6 8.4 f 0.01
24 32 32
26 45 33.5
Day 2 0400 h 1400 h 2200 h
8.0 k 2.8 5.3 * 2.1 7.0 k 1.6
4.3 * 0.7 3.0 * 1.0 1.9 f 0.5
24 40.5 30
26 46 31
Day 4 0400 h 1400 h 2200 h
6.0 + 0.001 1.7 f 0.71 3.7 + 1.22
1.6 i 0.5 2.0 * 0.3 2.0 ) 0.3
29 37 32
28 43 32
1.7 * 1.3 1.0 * 0.1
22 38
23 44
Day 7 04OOh 1400 h
5.33 k 0.60 1.33 f 0.71
collembolans were in the litter from 010&0800 h with a peak (x = 3 per 25 g) at 0400 h. Mites reported as “others” were primarily mites of the families Bdellidae and Stigmaeidae. There was no significant difference between total numbers of nematodes in soil or litter over the 24 h period and no evidence of diurnal migration (F = 1.64, P > 0.25) (Fig. 1). Seventy-eight to 98% of the nematodes were anhydrobiotic in both soil and litter at all times and there was no significant difference between the percentage of anhydrobiotic nematodes in soil or litter (F = 1.51, P > 0.25). The nematode taxa found in both the diurnal and stimulated bacteriophages--Acrobeles, rainfall studies were: Acrobeloides, Alaimus, Cephalobus, and Plectus; fungivores-Aphelenchus aoenae, Aphelenchoides, and Ditylenchus; omnivore predators-Dorylaimus, Prismatolaimus, and Pungentus; plant feeders-Tylenchorhynthus. Even following simulated rainfall when there were no marked decreases in litter or soil moisture content (Table l), there were fewer microarthropods in the litter at mid-day (Fig. 3). There were also significant reductions in numbers of active mites in the soil 4-8 days following the simulated rainfall when soil moisture dropped to approximately 2%. There was not only a reduction in total numbers of microarthropods during drying but there were marked decreases in species diversity (Shannon Weaver H’, Poole, 1974) litter: day 1, H’ = 1.85, day 2, 1.44, day 4, 0.90, day 8, 0.48. In soil on day 1 H’ = 1.71, day 2, 1.69, day 4, 1.95 and day 8,0.98. Surprisingly, the microarthropod diversity in the litter following natural rainfall was lower than that following simulated rainfall: day 1, H’ = 1.26, day 2, 1.48. In all samples, the measure of equitability was between 0.60 and 0.75. Although the numbers of microarthropods per unit of litter or soil were higher following natural rainfall than simulated rainfall (Fig. 3), the taxa and pattern of movement into the litter and soil were similar under both rainfall conditions. Oribatids and collembolans were active in the litter during days 1 and 2
following wetting. Tydeid mites were active in the surface litter for 50 h after rainfall (simulated or natural) and also in the shallow soil below the litter. The only animals that remained in the surface litter and shallow soil for more than 100 h following simulated or natural rainfall of 25 mm were nanorchestid mites (Fig. 4). Numbers of nematodes in the soil were not significantly different following the simulated rainfall experiment until day 8 at 0400 (Fig. 3) when there was a significant increase (F = 43.36, P < 0.01). Nematode numbers did not change significantly as the litter dried, or with the natural rainfall on day 8. The nematodes adapted physiologically to the drying soil and litter by coiling and entering anhydrobiosis. On day 1 at 0400, 35% of the nematodes were anhydrobiotic in the litter compared to 14% in the soil (Fig. 5). By 1400 h on day 1, 36 h following the simulated rainfall, 80% of the litter nematodes were anhydrobiotic. Soil nematodes did not become 807, anhydrobiotic until day 4 at 0400. After the natural rainfall on day 8, both soil and litter nematodes were 95-98x active (Fig. 5). There was no significant difference in abundance of bacteria in the litter from day 1 to day 4 after wetting, nor was there any significant difference in abundance of protozoans from day 1 to day 4 (Table 2). In the study of immediate (8 h) responses of microarthropods to simulated rainfall, there were marked increases in numbers and diversity of microarthropods in both litter and soil within 1 h of wetting. Although no collembolans were extracted from dry litter, the wet litter fauna was dominated by isotomid, sminthurid and onychiurid collembolans (Table 3). There were also increases in numbers and diversity of oribatids, tydeids and Bdella sp. There were some reductions in numbers and diversity in the litter fauna 8 h after wetting, but a greater reduction due to diurnal movement by microarthropods out of the litter in the 4 h samples collected at mid-day (Table 3). There was considerable variation in numbers and taxonomic composition at all sampling times in both wet and dry litter and soil samples (Tables 3 and 4).
421
Behavior of desert soil microfauna
0
PER
450
D
PER
259
0
LITTER
I
cm 3 SOIL LITTER
II
III
m
DAYS/HOURS Fig. 3. Changes in densities of soil and litter microarthropods (top panel) and nematodes (bottom panel) during 4 days following a simulated rainfall of 25.4 mm. Roman numerals indicate days after-wetting; arabic
numbers
indicate
time of day samples
were removed
was a marked reduction in microarthropods in the dry litter at 1200 h when its temperature was 44°C compared to 25’C in the wet litter. The wet litter contained 0.>2.0% moisture and the unamended soil 0.2% moisture throughout the study. There were fewer collembola in the soil than in the litter but dry soil had more microarthropods than the unwatered litter at 1200 h (Tables 3 and 4). There were similar reductions in microarthropods in the watered litter and soil at 1200 h despite the apparent moderate environmental conditions. There
DISCUSSION
Our studies reveal several behaviors of some of the biota inhabiting a desert litter-soil system. There was an apparent diurnal migration of microarthropods from soil into litter and back into soil during both dry
from the field. Vertical
lines equal
+ 1 SD.
conditions and after simulated rainfall. In dry litter these movements were correlated with changes in litter moisture and the temperatures of the litter soil interface. However, there were marked daily changes in numbers of microarthropods in litter and soil even when the system was moist following simulated rainfall. This suggests that the daily movements may reflect a type of circadian rhythm rather than a process triggered by microclimate. Water vapor which moves up through the soil during the day may condense on the leaf surfaces within litter aggregates when temperatures drop at night thus accounting for the higher litter moisture contents measured in the early morning. The phenomenon of water vapor movement in soil has been well documented in laboratory experiments (Jury and Letey, 1979). Syvertsen et al. (1975) suggested that anomalous stem water potentials in creosotebush Larrea
WALTER G. WHITFORDet ~1.
422
0 ORIBATIDS 0 NANORCHESTIDS A TYDEIDS
A COLLEMBOLA t 0 0 A
01
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4
14‘:
’
14
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22
0
A
A
0
A
0
A
0
0
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I
4
14
22
4
14
22
4
14
22
0
0
0A
0
.
n
A
W
0
A
n
A
0
4
14
22
a I
I
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n OTHER PREDATORY MITES
0
A
12 -
0
T E
EIO0 s: 6_ d $z-
*A 0
A
z ,I t
l
0
Lz
0 2-
0
0 0
”
4
H 14
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’
22
I
I
0 0
I
II
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I
I
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I
1
4
14
22
4
14
22
Ip
0 1 8
I
pm
II
8
mYIlI
DAYS Fig. 4. Changes in densities of selected taxa of microarthropods during rainfall of 25.4 mm. Roman numerals indicate days after wetting: arabic samples were removed from the field.
tridentata in a desert area near Las Cruces, New Mexico were due to movement of water vapor through the soil. We are not aware of any field studies in which water vapor movement has been measured in desert soils. Our data on changes in litter moisture contents may be regarded as presumptive evidence of this but litter could also absorb moisture from the air at high RH and low ambient temperatures. Obviously additional data are required to resolve this question. In laboratory experiments Metz (1971) showed that oribatids and mesostigmated mites moved from mineral soil into moist pine litter and that there was considerable mortality of the mites that moved into the litter upon subsequent drying. Some of the variation noted in our experiment may have been due to mortality but we attribute most of the changes in number to vertical migration.
8 days following numbers indicate
a simulated time of day
Oribatids and tydeids made up a large fraction of the mites migrating into the litter in the early morning. Whitford and Santos (1980) showed that decomposition of buried litter in North American hot deserts is a predator-controlled process and that tydeid mites are the most important predators of bacteriophagous nematodes in early stages of decomposition. Although tydeids were present in surface litter, oribatids were more numerous. Oribatids have been shown to affect decomposition by comminution of litter, grazing on fungi and inoculating litter with fungi (Edwards et al., 1970; Wallwork, 1970). We found that litter at a chihuanhuan desert site disappeared at high rates during May-July before any appreciable late summer rainfall (unpublished data). The diurnal migration and feeding by microarthropods especially Oribatids may be a significant factor in such litter
Table 2. Mean numbers of bacteria and protozoa in leaf litter following application simulated 25.4 mm rainfall. Samples collected at 0800 h Day 1 Cells g-’ Bacteria
litter
of a
Day 2 Cells m-’
Cells g-
1litter
Cells m _ ’
1.1 x 10B
8.48 x 10”
8.86 x 10’
6.69 x 10”
Protozoa Trophs Cysts
3.03 x lo4 2.45 x lo4
2.34 x lo8 1.89 x IO8
4.04 x lo4 7.05 x lo3
3.11 x 10” 5.44 x 10’
Total
5.48 x lo4
4.23 x lo*
4.74 x lo4
3.65 x 10’
423
Behavior of desert soil microfauna
3. Comparisons of abundances of litter microarthropods immediately after wetting and in unamended litter. Density reported as mean number f 1SD 30 g ’ litter. The number preceding h indicates number of hours elapsed since water applied and the time refers to the time the sample was collected
Table
Litter Taxon Collembola lsotomidae Onvchiurus sp. Sminthuridae
Litter dry
lh 0800
2h 0900
4h 1200
8h 0800
0800
1200
35.2 f 17.6 8.8 + 2.5 7.8 k 10.8
11.6 k 7.2 0.4 * 1.0 8.4 + 2.6
1.0 + 1.0 0 0.8 k 1.2
3.2 + 3.7 0 8.4 + 13.6
0 0 0
0 0 0
3.4 5.6 4.3 0.3 2.0
2.6 + 2.1 4.6 + 8.1 1.0 + 3.0 0 0
0.2 * 1.4 0 0 0 0
2.4 1.4 1.0 0.8 0.2
3.3 1.3 0.7 1.0 0.8
0.4 + 0.8 1.6 k 1.0 0.2 + 0.6 0 0
0 0 0 0 0
7.8 k 4.0 6.8 * 5.3 0
2.2 f 2.7 0 0
1.0 _I 0.7 0.6 k 0.5 5.6 k 3.2
0.2 k 0.8 0.2 * 1.0 0.2 + 0.8
0 0.2 * 1.0 0
1.2 + 2.0 1.0 0.2 0.8
0 0 1.4 * 1.9 3.8 + 0.8
1.2 + 2.0 0 0.2 * 1.2 0
0.2 k 0.8 0 0 0
0 0 0 0
Cryptostigmata Oribatei Pt7sx7~ozerrs
.sp.
Scheloribates .sp. Orihutula .sp. Gu/un7?717
cp.
Oppiu sp.
Prostigmata Tydeidae Bdellu sp. Nanorchestidae Mesostigmata Other mites Psocoptera Insect larvae
7.0 7.8 7.0 0.4 1.4
* k + + *
disappearance. Comminution and fungal grazing by microarthropods even for brief periods each day could result in rapid litter removal, thus, representing one of the most important processes in decomposition of surface litter in North American deserts. We had hypothesized that free-living nematodes would also migrate into the surface litter or a fraction of the anhydrobiotic nematodes would become active. There were no differences in numbers or the proportion of the population that was active at any time of the day. Therefore, it appears that changes of up to
Table 4. Comparisons
f * + k +
5% moisture in litter is insufficient to bring nematodes out of anhydrobiosis. There was a rapid shift from the anhydrobiotic to the active form after wetting. The lower rate of return to coiled forms in the soil in comparison to the litter reflects the more stable and slower drying moisture conditions of the soil. These relationships suggest that nematodes grazing on bacteria and fungi in desert surface litter is a brief process initiated by rain. However, the organic matter in shallow soil under litter provides a substrate for growth of microorganisms and a moist environment
of densities of soil microarthropods immediately after wetting, and in dry soil. Densities as the mean number + SD per 650 g of soil (81 cm2 surface area)
reported
Dry soil
lh 0800
2h 0900
4h 1200
8h 0800
0800
1200
Collembola Isotomidae Sminthuridae
0 0.8 + 0.9
0.2 + 1.0 0
0.7 * 0.5 0
0.4 + 1.0 0
0 0
1.0 f 1.0 0
Cryptostigmata Oribatei Passalozetes sp, Scheloribates Oributula sp. Oppia Other oribatids
0.6 k 0 0.6 k 1.4 f 2.1 k
0.9
0 0 0 0 0
0
1.0 1.0 2.5
1.2 Ifr 0.8 0 0.6 + 0.8 0 0.2 * 1.0
0.2 + 0.8 1.0 + 2.1 0 0.2 k 0.8
0.2 + 0.8 0 0 0 0
0 0 0 0 0.5 + 0.5
Prostigmata Tydeidae Bdella sp. Nanorchestidae Paratydeidae
0.6 0.4 0.2 1.8
k * + k
0.8 1.0 0.8 4.0
3.2 + 4.5 0.6 f 1.0 0 0
0 0 0.5 f 0.2 1.2 + 0.4
1.4 + 1.0 0.6 f 0.9 0.4 * 0.2 0
1.2 * 2.0 0.4 f 0.8 0.4 + 1.2 0
0 0 3.5 k 2.5 0
Other mites Mesostigmata Psocoptera Pauropoda Insect larvae
0.4 _t 0 0.2 * 0.2 * 0.2 *
0.8
0 0 0 0.2 * 1.0 0
2.5 + 1.3 2.4 k 2.1 0 0 0.4 +_ 0.6
1.8 k 1.0 0 0 0.6 + 0.9 0
0 0.4 + 1.0 0.2 * 1.0 0 0
1.5 * 1.0 0 0 0 0
Taxon
0.5 1.0 1.0
WALTER G. WHITFORDet al.
424
LITTER
100 -
20
80 -
G 0-I
16 60-
0
12
-
$? 40-
8
8
20-
4 0
12
:: _ -I
IO l
z
l
GO-
6
lu”
0 l
8
8
*
0
4020: 0
8
ft %
8
l
8
l
l
I
I
I
I
I
I
I
I
1
I
4
14
22
4
14
22
4
14
22
4
I
4
; z lx
l
II
l
m DAYS/
l
l
2
I
I
14
22
YUI
8
8
0
lx
HOURS
Fig. 5. The proportion (:I:) of the litter and soil nematode population in anhydrobiosis (coiled) following simulated rainfall. Roman numerals indicate days after wetting; arabic numbers indicate time of day samples were removed from the field. Open bars equal i SD.
for active face litter
nematodes. but spend
If microarthropods most of the time
feed on surin the soil. their
feces provides an energy source for microorganisms and indirectly to free-living nematodes. This represents a beneficial effect of microarthropods on nematodes in contrast to the predatorprey relationship found in buried litter. Thus, we suggest that grazing by free-living nematodes is more important in the soil than in the litter subsystem. Simons (1973) suggested that nematodes, due to diurnal fluctuations in soil moisture, might go in and out of anhydrobiosis. This would appear to be an appropriate mechanism for nematodes in deserts. However, this did not appear to be the case when we were sampling. Since nematodes can be induced to enter and leave the anhydrobiotic state in a short time (15 min to become active) perhaps we should compare active and anhydrobiotic nematode numbers every hour rather than at the sampling times used in this study. It is also possible that individual trophic groups, i.e. the bacterial feeders, may have become active and migrate in a short time. However, because of problems with preservation and extractions, we were unable to determine trophic group numbers. Although there was no significant change in numbers of protozoans or bacteria in the litter from day 1 to day 4 after wetting, this should not be construed as a lack of activity by these organisms. The technique used to count bacteria does distinguish live from dead cells and losses by grazing bacterivores can off-set increases due to cell division. The high propor-
tion of protozoan trophs in the dry litter may be an artifact of the technique because the temperature of the acid treatment was 22” not 5°C which may have resulted in the death of many cysts. While these data provide an estimate of the numbers of bacteria and protozoans present, more elaborate studies are necessary to examine their role in decomposition of desert surface litter. In the studies of immediate responses to simulated rainfall, the large numbers of microarthropods present in the litter 1 h after wetting (x total in wet litter = 93.2, x total in dry litter = 3.0) in contrast to the dry litter is indicative of either rapid migration from the soil or marked physiological change in the microarthropods. Some xeric-adapted species of Collembola have been shown to be capable of anhydrobiosis (Poinsot, 1968; Poinsot-Balaguer, 1976). The large numbers of Collembola extracted from wet litter and the complete absence of collembolans from the dry litter were taken as evidence of anhydrobiosis in these forms, but there are no reports of which we are aware of anhydrobiosis in mites. If the large numbers of oribatids, tydeids and bdellids migrated from the soil into the litter, they would have to have migrated from distances of more than 8cm (the depth of the core) in less than 1 h. The dry soil was virtually devoid of oribatids at 0800 h when large numbers of microarthropods were extracted from the wet litter and wet soil. Whatever the mechanism, these experiments demonstrate that the desert soil fauna responds rapidly to a single wetting. The activity of the desert
Behavior
of desert soil microfauna
soil microarthropods biota is obviously regulated by rainfall as suggested by Noy-Meir (1974) but as both the immediate response studies and other studies reported here show there is an important diurnal component to the activity patterns of the microfauna. Both diurnal movements between soil and litter and intense activity initiated by rainfall affect rates of litter disappearance. The relative contributions of these processes to litter disappearance requires additional study. A~lino~~/edgrment,s~This research National Science Foundation grant a U.S. National Science Foundation man.
supported by a U.S. to W. G. Whitford and grant to D. W. Freck-
REFERENCES
BABIUK L. A. and PAUL E. A. (1970) The use of fluorescein isothiocyanate in the determination of the bacterial biomass of a grassland soil. Canadian Journal of Microhiolog!, 16, 57-62. BIRCH H. R. (1958) The effect of soil drying on humus decomposition and nitrogen availability. PIant & Soil 10, 9_~31. BIRCH H. R. (1964) Mineralization of plant nitrogen following alternate wet and dry conditions. Plant & Soil 20, 43-49. DEMEURE Y., FRECKMAN D. W. and VAN GUNDY S. D. (1979) Anhydrobiotic coiling of nematodes in soil. Journal qf NenzAloloyJ 11, 189%195. EDWARDS C. A., REICHLE D. E. and CROSSLEY D. A. (1970) The role of soil invertebrates in turnover of organic matter and nutrients. In Analysis of Temperature Forest Eros~~stems(D. E. Reichle, Ed.), pp. 147-172. Ecological Studies, 16. Springer, Berlin. FKECKMAN D. W. and MANKAU R. (1977) Distribution and trophic structure of nematodes in desert soils. Ecological Builetin (Stockholm) 25, 51 l-514. FRECKMAN D. W.. MANKAU R. and FERRIS H. (1975) Nematode community structure in desert soils: tiema: tode recovery. Journal of Nematology 7, 343-346. FRECKMAN D. W., KAPLAN D. T. and VAN GUNDY S. D. (1977) A comparison of techniques for extraction and study of anhydrobiotic nematodes from dry soils. Journul of Nemurology 9, 176181.
425
JURY W. A. and LETEY J. JR (1979) Water vapour movement in soil: reconciliation of theory and experiment. Journal. Soil Science Society of America 43, 823-827. MCGREGOR A. N. (1972) Impact of wetting on microbial respiration in desert soil. Proceedings. Soil Science Society of America 36, 851-852. METZ L. J. (1971) Vertical movement of Acarina under moisture gradients. Pedobiologia 11, 262-268. NOIR-MEIR I. (1973) Desert ecosystems: environment and producers. Annual Review of Ecology and Systematics 4, 25-52. NOY-MEIR 1. (1974) Desert ecosystems: higher trophic levels. Annual Review of Ecology And Systemutics 5, 195-214. POINSOT N. (1968) Cas d’anhyrobiose chez le collembole Subisotoma cariabilis Gisin. Revue D’Ecologie et de Biologie du Sol 4, 585-586. POINSOT-BALAGUER N. (1976) Dynamique des communautes de Collemboles en milieu xerique mediterranean. Pedobiologia 16, l-17. POOLE R. W. (1974) An Introduction to Quantitative Ecology. McGraw-Hill, New York. PROP J. C. and NETSCHER C. (1978) Improved detection of low population densities of Meloidogyne. Nematologica 24, 129-232. SANTOS P. F., DEPREE E. and WHITFORD W. G. (1978) Spatial distribution of litter and microarthropods in a Chihuahuan desert ecosystem. Journal of Arid Environments 1, 4148. SIMONS W. R. (1973) Nematode survival in relation to soil moisture. Mededelingen van de Landbouwhogeschool te Wageningen 73, l-85. SINGH B. N. (1946) A method of estimating the numbers of soil protozoa especially amoebae, based on their differential feeding on bacteria. Annals of Applied Biology 33, 112-119. SYVERTSENJ. P., CUNNINGHAM G. L. and FEATHER T. V. (1975) Anomalous diurnal patterns of stem xylem potentials in Lurrea tridentata. Eco/ogy 56, 1423-1428. WALLWORK J. A. (1970) Ecoloyy of Soil Animals. McGrawHill, London. WHITFORD W. G. and SANTOS P. F. (1980) Arthropods and detritus decomposition in desert ecosystems. In Soil Biology as Related to Land Use Practice. Proceedings of the VII Znternational Colloquium of Soil Zoology (D: L. Dindal, Ed.), pp. 77&778. Office of Pesticide and Toxic Substances, EPA, Washington, DC.
voi 13. pp 417 to 425. 1981 Br,tam All right,, reserved
Copynght
0038-0717.‘b1.050417-09SO2.00~0 0 1981 Pergamon Press Ltd
DIURNAL MIGRATION AND RESPONSES TO SIMULATED RAINFALL IN DESERT SOIL MICROARTHROPODS AND NEMATODES WALTER G. WHITFORD, DIANA W. FRECKMAN’, NED Z. ELKINS, LAWRENCE W. PARKER, ROB PARMALEE’,JANICE PHILLIPS
and SUZANNE TUCKER Department of Biology, New Mexico State University, and ‘Department
of Nematology,
University
(Accepted
Las Cruces, NM 88003, U.S.A. of California, Riverside, CA 92521, U.S.A.
10 February
1981)
Summary-Diurnal
patterns of microarthropod abundance in surface leaf litter were related to its moisture content. Leaf litter moisture was nearly 7% by weight at 0800 h but fell to less than 1% by mid-day. Oribatid and tydeid mites moved into litter in the early morning and back into the soil before mid-day. There were no significant differences in numbers of nematodes in litter or soil and 78%98% of the nematodes were anhydrobiotic (coiled) in soil and litter at all times sampled. Following simulated rainfall there were fewer microarthropods in litter at mid-day in the absence of marked decreases in soil and litter moisture content. During drying, there were gradual reductions in numbers and species diversity of litter microarthropods. Nematode numbers did not change as litter dried. Anhydrobiotic nematodes in the soil increased from 14% on day 1 to 85% on day 4. Between 24 and 36 h after simulated rainfall, the proportion of anhydrobiotic litter nematodes increased from 35 to SO”l,,. Within I h after simulated rainfall, there were marked increases in numbers and diversity of microarthropods in surface litter. No collembolans were extracted from dry litter controls but the wet litter was dominated by isotomid, sminthurid and onychiurid collembolans. There were increases in numbers and diversity of oribatid, tydeid and gamasid mites in the wet surface litter within 1 h after wetting compared to controls.
INTRODUCTION Most desert ecosystem processes are regulated by rainfall (Noy-Meir, 1973, 1974). The frequency, amount and seasonal occurrences of rain, undoubtedly have varying effects on productivity, decomposition, population dynamics and behavior of the biota. The effect of rainfall on a process is dependent upon the time that process takes to respond. Because of the short time needed to initiate population growth of microorganisms, or to activate the microfauna, decomposition processes should exhibit rapid responses to wetting and drying. Few of these responses have been examined in desert ecosystems. Wetting and drying affects decomposition, microbial respiration and mineralization (Birch, 1958, 1964; McGregor, 1972). Little attention has been given to the dynamics of the soil biota during cycles following rainfall (Metz, 1971). In Chihuahuan desert ecosystems, organic matter is distributed in patches and the density and diversity of soil microarthropods varies as a function of litter quantity (Santos et al., 1978). Numbers of free-living nematodes are also higher in areas of litter accumulation under plants (Freckman and Mankau, 1977). As soon as the littersoil systems becomes rapidly and nitrogen
wet, organic is mineralized
matter decomposes (Birch, 1958, 1964)
1976) and may be activated by an increase in available moisture. Acarina may migrate from the moister environment of the mineral soil to litter (Metz, 1971). Prot and Netcher (1978) showed that Meloidogyne larvae in soil migrated 45 cm in 10 days to tomato roots suggesting that nematodes may undergo vertical migration in agricultural soils. Thus, the soil microfauna could respond to rainfall by vertical movements or activation from the anhydrobiotic state. Another process in desert litter-soil systems which may affect the behavior of the soil fauna is the movement and condensation of water vapor in the soil which results from diurnal heating and cooling. Because of the different thermal characteristics of litter with respect to soil, it is possible that water vapor which has moved up through the soil during the day may condense on the surfaces of leaves in the leaf litter at night. Thus, even in dry soil, diurnal differences in temperature or moisture could affect the behavior of the soil fauna. We report experiments designed to examine the behavior of a desert soil fauna in response to simulated rainfall. We also examined diurnal changes in soil and litter fauna in unwatered soil-litter systems. METHODS
suggesting a number of potential activities of the soil fauna. Some soil fauna (nematodes, tardigrades and collembola) are capable of anhydrobiosis (remaining alive in a dehydrated state with unmeasurably low metabolism) (Demeure et al., 1979; Poinsot-Balaguer,
Most of the studies were done on a site 13 km east of Las Cruces, New Mexico on a nearly flat peneplain of rocky, sandy-loam soil and sparse vegetation cover of creosotebush, Larrea tridentata (Cov.). Studies of 411
418
G.
WALTER
WHITFORD et al samples which were placed in modified Tullgren funnels to extract microarthropods. Nematodes were extracted from the remaining three litter and soil samples (see below). In the simulated rainfall experiments, 96 screen cylinders received the equivalent of 25.4 mm water. The wetting front in the soil below the litter expanded to an 18 cm circle. At 0400, 1400 and 2200 h, and on days 1, 2, 4 and 8 following the simulated rainfall, 8 cylinders were collected. Each sample consisted of the litter from the cylinder and a soil sample to 6 cm below the wet litter. Microarthropods were extracted from three samples and nematodes from the remaining five. Soil and litter temperatures were measured with a standard laboratory thermometer. Temperatures at the soil litter interface were recorded by carefully sliding the bulb under the litter along the soil surface until the bulb was covered. Soil temperatures were
immediate response to wetting were done 3 km east of Las Cruces, New Mexico on a site with deep sandy soil bearing a mixture of creosotebush and mesquite. Prosopis glandu/osa (Torr.). Litter was collected from under creosotebushes. The litter was approximately 60”/, creosotebush leaves with the remaining 407, annual plant parts, rabbit feces, mesquite leaves and parts of grasses. Twenty grams of litter for nematodes and 25 g of litter for other measurements was confined in open-bottom screen cylinders (9.8 cm dia) to prevent litter from being scattered. These quantities approximate the concentrations of litter normally found under shrubs in the area. The litter in the cylinders was left in the field for 6 days before simulated rainfall. Forty-eight cylinders were not given simulated rainfall. Six collections of these were made throughout 24 h at 0100, 0400, 0800, 1400, 1800 and 2200 h. Each collection consisted of five litter and five soil
.
SOIL-LITTER
INTERFACE
n MOISTURE
TEMPERATURE
BY WEIGHT
8
\
oI
I
I
2
I,
I,
4
‘I
6
I
6
I
10
I1
I
12
/-
‘m’ I
14
I
I
16
I
I
16
I
I
20
I,
I
22
24
HOURS
Fig. 1. Diurnal changes in numbers of microarthropods and nematodes extracted from soil and litter in relation to mean soil-litter interface temperature and mean litter moisture. The black bars below the time scale indicate periods of darkness, The top panel summarizes the data for nematodes with the height of the bar equalling the mean and the lines equalling & 1 SD. The middle panel summarizes the data for microarthropods with the height of the bar equalling the mean and the lines equalling + 1 SD.
Behavior
of desert soil microfauna
419
p NANORCHESTIOS IID OTHER MITES
0
0100
0400
1400
0600
1600
2200
HOUR
Fig. 2. Comparison
of mean numbers of different samples collected
by inserting the thermometer into the side of the bottom of the hole left when soil samples were removed. The samples for microarthropod extraction were collected into “ziplock” plastic bags, returned to the laboratory; microarthropods extracted in modified Tullgren funnels into water (Santos et al., 1978) and then counted. Subsamples were removed from these 25 g samples for litter moisture content and to estimate bacterial and protozoan numbers. Soil and litter moisture was determined by the gravimetric method (105°C for 24 h). Estimates of bacterial and protozoan numbers were made from the 1400 h samples on days 1 and 4 only. Bacterial numbers were estimated by direct counts using the FITC staining technique (Babiuk and Paul, 1970). Total and cystic protozoa were counted by the most-probable-number method (Singh, 1946). Cyst numbers were obtained by soaking 2g plant material in 2% HCl for 24 h at room temperature, the acid was neutralized and protozoan trophs were estimated as the difference between the total counts and cyst numbers. Nematode soil samples were taken beneath the litter with 7.5 cm dia oak field tube. Three samples each of litter and soil were mixed into containers of 5% formalin for later extraction of coiled and straight nematodes by the anhydrobiotic extraction technique (Freckman et a/., 1977). Two additional samples from both soil and litter were immediately placed in water for 12 h to obtain active, rehydrated nematodes, then preserved in 5% formalin for identification. Nematodes were extracted from litter and soil by a modified sugar floatation technique (Freckman et al., 1975) taken
taxa of microarthropods at the times indicated.
extracted
from litter and soil
but, most nematodes were unidentifiable due to in cico preservation in soil combined with the extraction technique. Initial results indicated that considerable activity developed immediately following a rain. In another set of experiments, the microarthropod fauna in litter and soil were compared l-8 h after wetting. We used 30 g litter moistened with the equivalent of 25.4 mm rainfall. Five replicates of each wet litter, dry litter, and upper 8 cm of soil under the litter were immediately returned to the laboratory and extracted. RESULTS
The diurnal movements of microarthropods into the surface litter was related to litter moisture and the litter-soil interface temperature (Fig. 1). Litter moisture reached nearly 7”/:, at 0800 h but fell rapidly to less than 1% by mid-day. There were significantly fewer microarthropods in the litter at 0400 and 1800 h (F = 15.8, P < 0.01). However, in the soil, the only significant reduction in numbers was at 2200 h (F = 5.38, P < 0.01). There was a significantly higher litter moisture at 0800 h than during the night (F = 15.8, P < 0.01). Some groups of Acarina moved from soil to litter and back into the soil. (Fig. 2). Oribatids moved into the litter in the early morning when temperatures at the soil litter interface were moderate and litter moisture was greater than 5% (Figs 1 and 2). Tydeid mites were in the litter when temperatures were moderate but apparently moved into the deeper soil at high temperatures. Tarsonemid mites (X = 3 per 25 g) were found only in litter samples from 0400 h. lsotomid
WALTERG. WHITFORDet al.
420
Table 1. Litter and soil moisture at 6cm (expressed as percent by weight); wet and dry soil temperatures following water amendment equivalent to 25.4mm. The percent moisture of the dry soil during the experiment was 0.55 + 0.01. On day 7 there was a natural rainfall of 25 mm at 1630 h Temperature Wetted soil
( C) Dry soil
Litter
Soil
Day 1 04OOh 1400h 2200 h
16.0 k 2.6 8.7 * 3.0 5.7 + 1.7
8.7 f 3.1 4.0 f 2.6 8.4 f 0.01
24 32 32
26 45 33.5
Day 2 0400 h 1400 h 2200 h
8.0 k 2.8 5.3 * 2.1 7.0 k 1.6
4.3 * 0.7 3.0 * 1.0 1.9 f 0.5
24 40.5 30
26 46 31
Day 4 0400 h 1400 h 2200 h
6.0 + 0.001 1.7 f 0.71 3.7 + 1.22
1.6 i 0.5 2.0 * 0.3 2.0 ) 0.3
29 37 32
28 43 32
1.7 * 1.3 1.0 * 0.1
22 38
23 44
Day 7 04OOh 1400 h
5.33 k 0.60 1.33 f 0.71
collembolans were in the litter from 010&0800 h with a peak (x = 3 per 25 g) at 0400 h. Mites reported as “others” were primarily mites of the families Bdellidae and Stigmaeidae. There was no significant difference between total numbers of nematodes in soil or litter over the 24 h period and no evidence of diurnal migration (F = 1.64, P > 0.25) (Fig. 1). Seventy-eight to 98% of the nematodes were anhydrobiotic in both soil and litter at all times and there was no significant difference between the percentage of anhydrobiotic nematodes in soil or litter (F = 1.51, P > 0.25). The nematode taxa found in both the diurnal and stimulated bacteriophages--Acrobeles, rainfall studies were: Acrobeloides, Alaimus, Cephalobus, and Plectus; fungivores-Aphelenchus aoenae, Aphelenchoides, and Ditylenchus; omnivore predators-Dorylaimus, Prismatolaimus, and Pungentus; plant feeders-Tylenchorhynthus. Even following simulated rainfall when there were no marked decreases in litter or soil moisture content (Table l), there were fewer microarthropods in the litter at mid-day (Fig. 3). There were also significant reductions in numbers of active mites in the soil 4-8 days following the simulated rainfall when soil moisture dropped to approximately 2%. There was not only a reduction in total numbers of microarthropods during drying but there were marked decreases in species diversity (Shannon Weaver H’, Poole, 1974) litter: day 1, H’ = 1.85, day 2, 1.44, day 4, 0.90, day 8, 0.48. In soil on day 1 H’ = 1.71, day 2, 1.69, day 4, 1.95 and day 8,0.98. Surprisingly, the microarthropod diversity in the litter following natural rainfall was lower than that following simulated rainfall: day 1, H’ = 1.26, day 2, 1.48. In all samples, the measure of equitability was between 0.60 and 0.75. Although the numbers of microarthropods per unit of litter or soil were higher following natural rainfall than simulated rainfall (Fig. 3), the taxa and pattern of movement into the litter and soil were similar under both rainfall conditions. Oribatids and collembolans were active in the litter during days 1 and 2
following wetting. Tydeid mites were active in the surface litter for 50 h after rainfall (simulated or natural) and also in the shallow soil below the litter. The only animals that remained in the surface litter and shallow soil for more than 100 h following simulated or natural rainfall of 25 mm were nanorchestid mites (Fig. 4). Numbers of nematodes in the soil were not significantly different following the simulated rainfall experiment until day 8 at 0400 (Fig. 3) when there was a significant increase (F = 43.36, P < 0.01). Nematode numbers did not change significantly as the litter dried, or with the natural rainfall on day 8. The nematodes adapted physiologically to the drying soil and litter by coiling and entering anhydrobiosis. On day 1 at 0400, 35% of the nematodes were anhydrobiotic in the litter compared to 14% in the soil (Fig. 5). By 1400 h on day 1, 36 h following the simulated rainfall, 80% of the litter nematodes were anhydrobiotic. Soil nematodes did not become 807, anhydrobiotic until day 4 at 0400. After the natural rainfall on day 8, both soil and litter nematodes were 95-98x active (Fig. 5). There was no significant difference in abundance of bacteria in the litter from day 1 to day 4 after wetting, nor was there any significant difference in abundance of protozoans from day 1 to day 4 (Table 2). In the study of immediate (8 h) responses of microarthropods to simulated rainfall, there were marked increases in numbers and diversity of microarthropods in both litter and soil within 1 h of wetting. Although no collembolans were extracted from dry litter, the wet litter fauna was dominated by isotomid, sminthurid and onychiurid collembolans (Table 3). There were also increases in numbers and diversity of oribatids, tydeids and Bdella sp. There were some reductions in numbers and diversity in the litter fauna 8 h after wetting, but a greater reduction due to diurnal movement by microarthropods out of the litter in the 4 h samples collected at mid-day (Table 3). There was considerable variation in numbers and taxonomic composition at all sampling times in both wet and dry litter and soil samples (Tables 3 and 4).
421
Behavior of desert soil microfauna
0
PER
450
D
PER
259
0
LITTER
I
cm 3 SOIL LITTER
II
III
m
DAYS/HOURS Fig. 3. Changes in densities of soil and litter microarthropods (top panel) and nematodes (bottom panel) during 4 days following a simulated rainfall of 25.4 mm. Roman numerals indicate days after-wetting; arabic
numbers
indicate
time of day samples
were removed
was a marked reduction in microarthropods in the dry litter at 1200 h when its temperature was 44°C compared to 25’C in the wet litter. The wet litter contained 0.>2.0% moisture and the unamended soil 0.2% moisture throughout the study. There were fewer collembola in the soil than in the litter but dry soil had more microarthropods than the unwatered litter at 1200 h (Tables 3 and 4). There were similar reductions in microarthropods in the watered litter and soil at 1200 h despite the apparent moderate environmental conditions. There
DISCUSSION
Our studies reveal several behaviors of some of the biota inhabiting a desert litter-soil system. There was an apparent diurnal migration of microarthropods from soil into litter and back into soil during both dry
from the field. Vertical
lines equal
+ 1 SD.
conditions and after simulated rainfall. In dry litter these movements were correlated with changes in litter moisture and the temperatures of the litter soil interface. However, there were marked daily changes in numbers of microarthropods in litter and soil even when the system was moist following simulated rainfall. This suggests that the daily movements may reflect a type of circadian rhythm rather than a process triggered by microclimate. Water vapor which moves up through the soil during the day may condense on the leaf surfaces within litter aggregates when temperatures drop at night thus accounting for the higher litter moisture contents measured in the early morning. The phenomenon of water vapor movement in soil has been well documented in laboratory experiments (Jury and Letey, 1979). Syvertsen et al. (1975) suggested that anomalous stem water potentials in creosotebush Larrea
WALTER G. WHITFORDet ~1.
422
0 ORIBATIDS 0 NANORCHESTIDS A TYDEIDS
A COLLEMBOLA t 0 0 A
01
’
4
14‘:
’
14
’
22
0
A
A
0
A
0
A
0
0
I
I
I
I
I
I
4
14
22
4
14
22
4
14
22
0
0
0A
0
.
n
A
W
0
A
n
A
0
4
14
22
a I
I
I
n OTHER PREDATORY MITES
0
A
12 -
0
T E
EIO0 s: 6_ d $z-
*A 0
A
z ,I t
l
0
Lz
0 2-
0
0 0
”
4
H 14
I
’
22
I
I
0 0
I
II
I
I
I
I
I
1
4
14
22
4
14
22
Ip
0 1 8
I
pm
II
8
mYIlI
DAYS Fig. 4. Changes in densities of selected taxa of microarthropods during rainfall of 25.4 mm. Roman numerals indicate days after wetting: arabic samples were removed from the field.
tridentata in a desert area near Las Cruces, New Mexico were due to movement of water vapor through the soil. We are not aware of any field studies in which water vapor movement has been measured in desert soils. Our data on changes in litter moisture contents may be regarded as presumptive evidence of this but litter could also absorb moisture from the air at high RH and low ambient temperatures. Obviously additional data are required to resolve this question. In laboratory experiments Metz (1971) showed that oribatids and mesostigmated mites moved from mineral soil into moist pine litter and that there was considerable mortality of the mites that moved into the litter upon subsequent drying. Some of the variation noted in our experiment may have been due to mortality but we attribute most of the changes in number to vertical migration.
8 days following numbers indicate
a simulated time of day
Oribatids and tydeids made up a large fraction of the mites migrating into the litter in the early morning. Whitford and Santos (1980) showed that decomposition of buried litter in North American hot deserts is a predator-controlled process and that tydeid mites are the most important predators of bacteriophagous nematodes in early stages of decomposition. Although tydeids were present in surface litter, oribatids were more numerous. Oribatids have been shown to affect decomposition by comminution of litter, grazing on fungi and inoculating litter with fungi (Edwards et al., 1970; Wallwork, 1970). We found that litter at a chihuanhuan desert site disappeared at high rates during May-July before any appreciable late summer rainfall (unpublished data). The diurnal migration and feeding by microarthropods especially Oribatids may be a significant factor in such litter
Table 2. Mean numbers of bacteria and protozoa in leaf litter following application simulated 25.4 mm rainfall. Samples collected at 0800 h Day 1 Cells g-’ Bacteria
litter
of a
Day 2 Cells m-’
Cells g-
1litter
Cells m _ ’
1.1 x 10B
8.48 x 10”
8.86 x 10’
6.69 x 10”
Protozoa Trophs Cysts
3.03 x lo4 2.45 x lo4
2.34 x lo8 1.89 x IO8
4.04 x lo4 7.05 x lo3
3.11 x 10” 5.44 x 10’
Total
5.48 x lo4
4.23 x lo*
4.74 x lo4
3.65 x 10’
423
Behavior of desert soil microfauna
3. Comparisons of abundances of litter microarthropods immediately after wetting and in unamended litter. Density reported as mean number f 1SD 30 g ’ litter. The number preceding h indicates number of hours elapsed since water applied and the time refers to the time the sample was collected
Table
Litter Taxon Collembola lsotomidae Onvchiurus sp. Sminthuridae
Litter dry
lh 0800
2h 0900
4h 1200
8h 0800
0800
1200
35.2 f 17.6 8.8 + 2.5 7.8 k 10.8
11.6 k 7.2 0.4 * 1.0 8.4 + 2.6
1.0 + 1.0 0 0.8 k 1.2
3.2 + 3.7 0 8.4 + 13.6
0 0 0
0 0 0
3.4 5.6 4.3 0.3 2.0
2.6 + 2.1 4.6 + 8.1 1.0 + 3.0 0 0
0.2 * 1.4 0 0 0 0
2.4 1.4 1.0 0.8 0.2
3.3 1.3 0.7 1.0 0.8
0.4 + 0.8 1.6 k 1.0 0.2 + 0.6 0 0
0 0 0 0 0
7.8 k 4.0 6.8 * 5.3 0
2.2 f 2.7 0 0
1.0 _I 0.7 0.6 k 0.5 5.6 k 3.2
0.2 k 0.8 0.2 * 1.0 0.2 + 0.8
0 0.2 * 1.0 0
1.2 + 2.0 1.0 0.2 0.8
0 0 1.4 * 1.9 3.8 + 0.8
1.2 + 2.0 0 0.2 * 1.2 0
0.2 k 0.8 0 0 0
0 0 0 0
Cryptostigmata Oribatei Pt7sx7~ozerrs
.sp.
Scheloribates .sp. Orihutula .sp. Gu/un7?717
cp.
Oppiu sp.
Prostigmata Tydeidae Bdellu sp. Nanorchestidae Mesostigmata Other mites Psocoptera Insect larvae
7.0 7.8 7.0 0.4 1.4
* k + + *
disappearance. Comminution and fungal grazing by microarthropods even for brief periods each day could result in rapid litter removal, thus, representing one of the most important processes in decomposition of surface litter in North American deserts. We had hypothesized that free-living nematodes would also migrate into the surface litter or a fraction of the anhydrobiotic nematodes would become active. There were no differences in numbers or the proportion of the population that was active at any time of the day. Therefore, it appears that changes of up to
Table 4. Comparisons
f * + k +
5% moisture in litter is insufficient to bring nematodes out of anhydrobiosis. There was a rapid shift from the anhydrobiotic to the active form after wetting. The lower rate of return to coiled forms in the soil in comparison to the litter reflects the more stable and slower drying moisture conditions of the soil. These relationships suggest that nematodes grazing on bacteria and fungi in desert surface litter is a brief process initiated by rain. However, the organic matter in shallow soil under litter provides a substrate for growth of microorganisms and a moist environment
of densities of soil microarthropods immediately after wetting, and in dry soil. Densities as the mean number + SD per 650 g of soil (81 cm2 surface area)
reported
Dry soil
lh 0800
2h 0900
4h 1200
8h 0800
0800
1200
Collembola Isotomidae Sminthuridae
0 0.8 + 0.9
0.2 + 1.0 0
0.7 * 0.5 0
0.4 + 1.0 0
0 0
1.0 f 1.0 0
Cryptostigmata Oribatei Passalozetes sp, Scheloribates Oributula sp. Oppia Other oribatids
0.6 k 0 0.6 k 1.4 f 2.1 k
0.9
0 0 0 0 0
0
1.0 1.0 2.5
1.2 Ifr 0.8 0 0.6 + 0.8 0 0.2 * 1.0
0.2 + 0.8 1.0 + 2.1 0 0.2 k 0.8
0.2 + 0.8 0 0 0 0
0 0 0 0 0.5 + 0.5
Prostigmata Tydeidae Bdella sp. Nanorchestidae Paratydeidae
0.6 0.4 0.2 1.8
k * + k
0.8 1.0 0.8 4.0
3.2 + 4.5 0.6 f 1.0 0 0
0 0 0.5 f 0.2 1.2 + 0.4
1.4 + 1.0 0.6 f 0.9 0.4 * 0.2 0
1.2 * 2.0 0.4 f 0.8 0.4 + 1.2 0
0 0 3.5 k 2.5 0
Other mites Mesostigmata Psocoptera Pauropoda Insect larvae
0.4 _t 0 0.2 * 0.2 * 0.2 *
0.8
0 0 0 0.2 * 1.0 0
2.5 + 1.3 2.4 k 2.1 0 0 0.4 +_ 0.6
1.8 k 1.0 0 0 0.6 + 0.9 0
0 0.4 + 1.0 0.2 * 1.0 0 0
1.5 * 1.0 0 0 0 0
Taxon
0.5 1.0 1.0
WALTER G. WHITFORDet al.
424
LITTER
100 -
20
80 -
G 0-I
16 60-
0
12
-
$? 40-
8
8
20-
4 0
12
:: _ -I
IO l
z
l
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lu”
0 l
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8
*
0
4020: 0
8
ft %
8
l
8
l
l
I
I
I
I
I
I
I
I
1
I
4
14
22
4
14
22
4
14
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4
I
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; z lx
l
II
l
m DAYS/
l
l
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I
I
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YUI
8
8
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HOURS
Fig. 5. The proportion (:I:) of the litter and soil nematode population in anhydrobiosis (coiled) following simulated rainfall. Roman numerals indicate days after wetting; arabic numbers indicate time of day samples were removed from the field. Open bars equal i SD.
for active face litter
nematodes. but spend
If microarthropods most of the time
feed on surin the soil. their
feces provides an energy source for microorganisms and indirectly to free-living nematodes. This represents a beneficial effect of microarthropods on nematodes in contrast to the predatorprey relationship found in buried litter. Thus, we suggest that grazing by free-living nematodes is more important in the soil than in the litter subsystem. Simons (1973) suggested that nematodes, due to diurnal fluctuations in soil moisture, might go in and out of anhydrobiosis. This would appear to be an appropriate mechanism for nematodes in deserts. However, this did not appear to be the case when we were sampling. Since nematodes can be induced to enter and leave the anhydrobiotic state in a short time (15 min to become active) perhaps we should compare active and anhydrobiotic nematode numbers every hour rather than at the sampling times used in this study. It is also possible that individual trophic groups, i.e. the bacterial feeders, may have become active and migrate in a short time. However, because of problems with preservation and extractions, we were unable to determine trophic group numbers. Although there was no significant change in numbers of protozoans or bacteria in the litter from day 1 to day 4 after wetting, this should not be construed as a lack of activity by these organisms. The technique used to count bacteria does distinguish live from dead cells and losses by grazing bacterivores can off-set increases due to cell division. The high propor-
tion of protozoan trophs in the dry litter may be an artifact of the technique because the temperature of the acid treatment was 22” not 5°C which may have resulted in the death of many cysts. While these data provide an estimate of the numbers of bacteria and protozoans present, more elaborate studies are necessary to examine their role in decomposition of desert surface litter. In the studies of immediate responses to simulated rainfall, the large numbers of microarthropods present in the litter 1 h after wetting (x total in wet litter = 93.2, x total in dry litter = 3.0) in contrast to the dry litter is indicative of either rapid migration from the soil or marked physiological change in the microarthropods. Some xeric-adapted species of Collembola have been shown to be capable of anhydrobiosis (Poinsot, 1968; Poinsot-Balaguer, 1976). The large numbers of Collembola extracted from wet litter and the complete absence of collembolans from the dry litter were taken as evidence of anhydrobiosis in these forms, but there are no reports of which we are aware of anhydrobiosis in mites. If the large numbers of oribatids, tydeids and bdellids migrated from the soil into the litter, they would have to have migrated from distances of more than 8cm (the depth of the core) in less than 1 h. The dry soil was virtually devoid of oribatids at 0800 h when large numbers of microarthropods were extracted from the wet litter and wet soil. Whatever the mechanism, these experiments demonstrate that the desert soil fauna responds rapidly to a single wetting. The activity of the desert
Behavior
of desert soil microfauna
soil microarthropods biota is obviously regulated by rainfall as suggested by Noy-Meir (1974) but as both the immediate response studies and other studies reported here show there is an important diurnal component to the activity patterns of the microfauna. Both diurnal movements between soil and litter and intense activity initiated by rainfall affect rates of litter disappearance. The relative contributions of these processes to litter disappearance requires additional study. A~lino~~/edgrment,s~This research National Science Foundation grant a U.S. National Science Foundation man.
supported by a U.S. to W. G. Whitford and grant to D. W. Freck-
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