- Email: [email protected]
Observations on the macro-fungi of an apple orchard in relation to cover crops and NPK fertilizers
[ 4°3 ] Trans. Br. "!)Icol. Soc. 58 (3), 403-416 (197 2) Printed in Great Britain
OBSERVATIONS ON THE MACRO-FUNGI OF AN APPLE ORCHARD IN RELATION TO COVER CROPS AND NPK FERTILIZERS By T. E. T. BOND
University
of Bristol, c/o Long Ashton Research Station (With 3 Text-figures)
A study of sporophore production by the higher fungi on experimental apple orchard swards was made on the basis of observations at approximately 10-day intervals during the season, fromJuly 1963 until the end of 1968. In all, some 27 species were recorded, with a total fresh-weight productivity estimated to be ofthe ordet of I - I 0 kg/ha/year. By far the most abundant was the summerfruiting Panaeolinafoenisecii (Pers. ex Fr.) Maire. Productivity and mid-dates of fruiting of this and certain other species were studied in relation to the different types of sward (established from seed in 1955) and to factorial applications of NPK fertilizers, but few significant responses were observed. The records were also exantined in relation to meteorological data as summarized for the early, mid- and late lo-day periods in each month.
The grass orchard sward is a type of semi-permanent artificial grassland which, under modern conditions in this country, is maintained by mowing rather than by the grazing animal. In this respect it may be compared with lawns and other recreational grasslands. There are far fewer species of higher fungi in these vegetational communities than in woodlands or in the more' natural' grasslands and heaths, and their fruiting is in general less conspicuous. Their ecology has been little studied. This paper is an account of 5 (6) years' observations on the higher fungi of a long-standing cover crop and manurial experiment in an apple orchard at Long Ashton. The objectives were to find out what fungi were fruiting in the area, their total and relative abundance and seasonal productivity, their changing behaviour from year to year and their response to the experimental treatments. As will become apparent, the observed effects of the experimental treatments were slight and the results are presented mainly as a record of an intensive survey of the macro-fungal flora of the area in question. THE EXPERIMENTAL ORCHARD
The site and experimental layout were fully described by Bould & Jarrett (1962). The orchard (Nat. Grid ref. ST 534.695) is situated in a shallow E.-W. valley at an altitude of c. 47 m. The soil is a reddish brown imperfectly drained deep loam derived from interbedded Triassic marl and sandstones geologically classifiable as Keuper Marl (Cope, 1970). The site before planting in 1952 had been under continuous arable
404
Transactions British Mycological Society
cultivation for at least 30 years. The planting consists of the three apple varieties: Cox's Orange Pippin, Worcester Pearmain and Bowden's Seedling, planted at 20 ft (6· I m) square with consecutive rows of each variety running from north to south. The trees are all on Malling II stock, and have been trained into delayed open-centre form with a free trunk of about 0·8 m. For the first 3 years after planting the ground was cultivated during the spring and summer, weeds being allowed to grow during the autumn. The cover crops (see below) were sown in April 1955 and the whole area since then has been regularly mown as required, the mowings being left to decompose in situ. During the years under review an area of about 4 m 2 around the base of each trunk has been sprayed with paraquat weedkiller. In addition to the experimental applications of fertilizer, an overall spring dressing of Nitro-chalk has been given yearly. The whole orchard receives a routine commercial spray programme for pest and disease control. The experimental area, a rectangular block of 25 rows of 17 trees, comprises the greater part of the orchard in which it is situated; it covers about Ii hectares (see Fig. I). The four sub-blocks of the layout divide it equally in both directions. Each sub-block comprises four cover crop (main) plots arranged side by side - a full row of 17 trees thus extends over two main plots. For recording purposes, only the even-numbered trees of the varieties Cox and Worcester are used; the third variety, Bowden's Seedling, forms the N.-S. buffer rows. Thus, each main plot consists offour pairs of recorded trees; each pair, buffered on all sides by guard trees, represents a single sub-plot. The experiment involves four cover-crop treatments (swards), with eight fertilizer (NPK factorial) treatments superimposed, the layout being a randomized block design with partially confounded split plots giving fourfold replication of the main (cover crop) plots and eightfold replication of the sub- (fertilizer) plots. The cover crop treatments comprise one natural sward (' tumbledown', not seeded) and three swards established from seed, respectively, of wild white clover (Trifolium repens), perennial ryegrass (Lolium perenne) and timothy grass (Phleum pratense). Despite the use of selected Aberystwyth 'leafy' strains of the two seeded grass species, already by 1960 (Bould & Jarrett, 1962) there had been a considerable levelling out of the initial sward differences as a result of progressive invasion by Agrostis stolonifera and other grasses indigenous to the locality, and of the natural spread of wild white clQver. Now, some IOyearslater,itseems likely that a still greater uniformity of the swards has been reached, although the perennial rye- and timothy-grass plots are still fairly readily identifiable. The fertilizer (sub-plot) treatments are based on annual applications of Nitro-chalk (15 % N), superphosphate (18 % P 20 S) and potassium sulphate (48 % K 20) at 250, 375 and 125 kgjha respectively, these applications being superimposed on the main plots in combination (a), N: P: K :NPK, or (b), NP: NK: PK: Nil. Since 1967 the experiment has been modified to include the comparison between sward cover and a weedfree environment. This has involved applying herbicide (paraquat and simazine), overall, to half of the plots, and has correspondingly reduced the area of sward available for recording the fungi.
Productivity of macro-Jungi. T. E. T. Bond
405
RECORDING THE FUNGI
Numbers and identity offungal sporophores were recorded on the basis ofsingle' plots' defined as the area ofsward surrounding a pair of recorded trees as far as the mid-line between these and the adjacent guard trees (but excluding the area treated with paraquat around the base of each tree). The procedure was to walk up and down between the Cox and Worcester rows, encircling each tree of the recorded pair in an anticlockwise direction, collecting all sporophores from the sward and discarding them across the plot boundaries. The ground was traversed either a whole row at a time, starting at random from either end of the area or working outwards from the middle, or in half rows taking the sub-blocks of the experiment in random order. Recording commenced in July 1963 and was continued until the end of 1968; from 1964 onwards a full survey was made on the average about 18 times a year at approximately lO-day intervals from the middle of May until the end of November. The main work used for identification was that ofKlihner & Romagnesi (1953). In the account which follows the agaric nomenclature is in accordance with the' New Check List . ..' of Dennis, Orton & Hora (1960) : 'treated' plots are those sprayed overall with herbicide in 1967: the four 'cover crop' treatments are designated W (wild white clover), X (perennial rye grass), r (timothy grass) and Z ('tumble-down'). THE MACROFUNGAL FLORA
Specific frequencies and total sporophore production Table I summarizes the records for the full 5-year period, 1964-8. A total of 24 species is included (or 27 species, if the incomplete records for 1963 are taken into account) of which the first five may be regarded as 'constants' for the experimental area (Wilkins & Patrick, 1939), found in at least a quarter of the individual plots and recorded in at least four years out of the five. The remainder, except possibly for Agaricus campestris, may be regarded as the 'sporadic' element. The close correspondence between specific frequency and total sporophore production is noteworthy, as is the overwhelming preponderance of the single species Panaeolina foenisecii. No direct measurements of weight were made at the time of recording, but observations subsequently have indicated that the yearly average fresh weight production represented by the data in the Table is of the order of 1-10 kg/ha.
rear?J recurrence and persistence The high proportion of 'sporadics' in the mycoflora means that the number of species recorded in anyone year is likely to fall considerably short of the total for the area in question. Thus, Table 2 shows that even in the most favourable years the number of species recorded was only some 60 % ofthe 5-yearly total; and, too, the figures suggest that the cumulative total is still subject to increase. Particular interest attaches to certain species of localized distribution
406
Transactz"ons Brz"tz"sh Mycologz"cal Soaety Table
I.
Occurrence offungi, their specific frequency and total sporophore production, 1964-8
A: 32 ('untreated') plots only, for all 5 years; 3937 sporophores (19 spp.). B: All 64 plots, for 3 years; then 32 ('untreated') plots, for 2 years; 6389 sporophores (24 spp.). (A)
(B)
r - -_ _....J>A
PaTUUlolinafoenisecii* Conocybe lactea* C. tenera agg.* Coprinus plicatilis* C. lagopus Agaricus campestris* Agtocybe semwrbicularis* Lepwta aistata* Lycopetdon depressum Bon.* Marasmius graminum* Clitocybe dealbata* Mycena aetites* Agrocybe praecox Galerina cZavata Coprinus friesii Psathyrella atornata Bolbitius vitellinus Eccilia camrina Bovistaplumbea Fr.* Panaeolus ater Mycena sepia* Omphalina velutina (?) Stropharia coronilla Tubaria conspersa (?)
--.,
, r - - - . . AA- - - - - ,
Occurrence (in years out of 5)
Frequency (in plots out of 32)
Total sporophares
Frequency (in plots out of 64)
Total sporophares
5* 4* 5 4* 4* 4* 2* 3* 2* 3* 2* 1*
32 27 23 22
3 19 1 269 160 159 35 34 22 7 5 20
63 47 48 43 19 9 4 10 3 5
493 1 506 302 303 50 47 60 18 7 76
2
7
3
10
I
II
2
14
I I I I 1
I I I I I
10 2 I 1 I
It I 2 I 1
10 2
1 1*
1
I
1
I
I
I
It 1
II
6 3 3 3 2
9 I I I
1*
I
2
3
17 15 7
I
I
2
I
I
I
I
* Recorded also in 1963 (with Agrocybe temulenta, Conocybe plicatella and Coprinus hemerobius). t In 1968 only, i.e. 1/32.
which may afford evidence of persistence from year to year. Notes on four such species are given below, and the occurrence of the first three of these is indicated in diagrammatic fashion in Fig. 1. Agaricus campestris. Recorded on, or just over the boundary of, 16 plots of which 11 were mutually adjacent in the S.E. corner ofthe area. In these 16 plots a total of 38 yearly occurrences was noted in the period 1963-8 inclusive, representing an average constancy/plot of 2'375 years in six, or nearly 40 %. Sporophores were not recorded in any of the plots in 1965 or in 1967; in three plots they were recorded for each of the remaining 4 years, in four plots for 3 years, in five plots for 2 years and in four plots for a single year only. Clitocybe dealbata. Apparently associated with A. campestris; in five plots only, four of them with records of the latter species in the same year as the Clitocybe, one with records of it in the previous year and again in the year following. Coprinus lagopus. Recorded from 19 plots, with a total of 26 yearly occurrences, making an average constancy/plot of 1'37 years in five (27 %); no great evidence ofpersistence on the plots individually, although
Productivity of macro-fungi. T. E. T. Bond
16 14
.. •
J
~
10 ~
0
8
6 4
2-
J
I
4
,
I
• •
.'
0
0
0
0
0
o~
0
0 ,0
J
10
13 Rows
,
0 0
0
0
7
, ,
I
I
0
I
I
I
• V • •
12
b
.1 IyV V
I
,
16
•
6
0 , ,0
I
,
I-
25
19
I
50m
Fig. I. Sketch plan of experimental area with position of individual plots, showing occurrence of Agaricus campestris (e), Clitocybe dealbata (f) and Coprinus lagopus (0).
Table 2. Numbers oj species ojfungi recorded, Ig63-8 (Cumulative totals in parentheses. A: 32 ('untreated') plots only, 1964-8. B: All 64 plots, 1964-6. C: As 'B', with the preliminary data from July 1963.) B A 1963 1964 196 5 1966 196 7 1968
8 (8)
12 (12)
II (12) II (16)
14 (17) 13 (22)
5 (17) 9 (19) Total recorded area, 64 plots - 0·43 ha.
the marked westerly distribution in the area as a whole (Fig. I) has still to be accounted for. Marasmius graminum. This little (epiphyllous) species was recorded from five plots only; in one of them for 2 years running and in one for two years with a gap of a year between them.
Times ojfruiting Subdividing the fruiting season into lo-day periods ending 20,30 May, gJune, ...,6, 16 and 26 November allowed for the records of sporophore M YC
58
Transactions British Mycological Society I ~'J; I Jilin: I 'II'" I ~1I~. I .' 'p:. I :XII
40 8
\'
t (~ \ II.) .
PI/I/(I('o!il/I/
/f1('II/\ecii
I/prtl/II 11/fl,°PIII
t~ t [
-
(13.
']
\'11.)
Clllwnh(' lI/c/('/1
C.ll!l/l!ra
-
=
(2 . \ III.) Copriml\ p!icuttli
Al!aricll~ F C(lII/Pl·.
lri~
E
.(.. (30.
\'III )
-
Fig. 2. Numbers ofsporophores in lo-day periods, 1964-8, as percentages of the total, with mid-dates offruiting.
production to be reassembled under 'early', 'mid-' and 'late' IO-day periods in each calendar month. This was done, for the population as a whole and for the six principal species, as shown in Fig. 2. The mid-dates offruiting are also given, determined from the average intervals to fruiting in days from May 20 as the starting-point (Richardson, 1970). The overwhelmingly aestival aspect of this particular macrofungal population
Productivity of macro-fungi. T. E. T. Bond
409
is indicated by the occurrence, in each of the 5 years 1964-8, of at least 90 % of the total sporophores during the period from late May to late August inclusive; or, in the 5 years together, ofjust over 95 % of the total from early June to mid-August inclusive. This of course reflects the preponderance of Panaeolina foenisecii (77 % of the total sporophores), with its mid-date of fruiting falling between early June (in 1964) and early July (1968), but even so it should be noted that for none of the other principal species does the mid-date of fruiting occur later than the end of August. The two species with the most extended fruiting season are Conocybe tenera and Coprinus plicatilis; in 1964 there was a pronounced 'flush' of the delicate sporophores of the Coprinus during mild weather in late November (see below).
Annual variation Annual variation in the number of sporophores recorded for the principal species is shown in Table 3. An attempt was made to interpret the yearly and seasonal differences in productivity in terms of meteorological factors of which the most significant appeared likely to be rainfall, maximum and minimum air temperature, relative humidity, temperature of the soil at IO cm depth and date of the first autumn frosts. For this purpose the Research Station's meteorological data for each of the 5 years were averaged over lo-day periods and a close visual comparison made with the fruiting records for the same periods (see above). The year 1967, in which the normally most abundant species scarcely fruited at all, was immediately identifiable meteorologically as having the lowest summer (June-August) rainfall of the years in question and the highest autumn (September-November) rainfall. In the summer of that year there was complete drought in both early and mid-June and virtual drought (1'75 mm rain) in earlyJuly and again (0'25 mm) in late August; during the autumn there was exceptionally heavy rain in each of the five consecutive IO-day periods from late September onwards. It is suggested that the predominant summer-fruiting species were largely prevented from fruiting by drought and that some of the more delicate sporophores of such later species as Conocybe tenera and Coprinus plicatilis may have been missed due to mechanical damage caused by the heavy rain or to concealment by the excessive growth of the herbage. For the other 4 years only some very tentative relationships are suggested, as indicated below under the several species: Panaeolina foenisecii. In the peak year, 1966, fruiting was not only exceedingly prolific but it was also unusually concentrated, with 91 % of the total sporophores collected being gathered on two occasions a week apart, in late June. Rainfall during May, June and July of that year was about average, and well distributed, but the soil temperature and maximum air temperature for early June, the minimum air temperature for mid-June and the relative humidities for mid- and late June were all the highest for their respective IO-day periods in any of the years in question. Conceivably, conditions for fruiting of P. foenisecii were so exceptionally favourable that year during June that the fruiting potential of the majority of the mycelia in the soil was exhausted in producing a single exceptionally 29-2
4 10
Transactions British Mycological Society Table 3. Yearly production of sporophores by principal species (Thirty-two plots for 5 years, 1964-8)
Panaeolina foenisecii (mid-date of fruiting) Conocybe lactea (mid-date of fruiting) Conocybe tenera Coprinus plicatilis C. lagopus Agaricus campestris All species
1964 200 (13. vi) 53 (19. vii) 15 66 8 21 37 1
1965 848 (26. vi) 115 (17. vii) 19 56 10 1061
1966
196 7
1328 (27. vi) 98 (4. vii) 114 25 14 5 1601
II
(3. viii) 4 6 42
1968 804 (2. vii) 3 (26. vi) 8 12 3 2 862
large flush ofsporophores towards the end of that month. In 1964 fruiting may possibly have been hastened by the occurrence of above-average soil temperatures for each of the IO-day periods in May and then curtailed by a period of drought in late June; in 1968, it may have been delayed by inadequate rainfall in the early and mid-June periods. Conorybe lactea. The high yield in 1965 was mainly concentrated in a single flush with its peak, in mid-July, following a peak in rainfall of about a month earlier. No such relationship was apparent in 1966. In 1968 there was exceptionally heavy rain (130 mm in 24 h) in mid-July and the only sporophores recorded during the year were a few early ones from the two previous periods. C. tenera. The peak yield in 1966 occurred in three quite distinct flushes, in mid- and late May, in early and mid-August and in mid- and late October respectively. No similar periodicity was apparent in the meteorological data. Coprinus plicatilis. The 1964 season was unusually prolonged, with the last collection of sporophores on 19 November. In that year the pattern of fruiting, with apparently six distinct flush periods, followed closely the pattern of rainfall. The prolonged autumn season was associated with the virtual absence of frost until 30 November and with the occurrence, in both mid- and late November, of above-average air maximum and minimum temperatures and soil temperatures (Fig. 3). C. lagopus. In 1968, these very delicate rather ephemeral sporophores may have been under-recorded following the torrential rain in mid-July (see above). Agaricus campestris. The high yield in 1964 occurred mainly between mid-August and late September. In that year, the soil temperatures and maximum air temperatures for late July and early August were the highest for any of the years in question, as were the maximum air temperatures throughout September, and the rainfall from July onwards, though below average in amount, was well distributed.
Productivity of macro-fungi. T. E. T. Bond
20
6:T E .
.--'--
80
15
/'-..
~l o (/)
.--'-
/
../
"'. "'-
._.""",
13. x.
II. xi. 30. xi.
\~-j~
10
70
411
1 1
60
IE ~ -
50 90 40
~'()
•
~O
60
30
50 40
I
110 G~O
<:
E
~
~ r,;:<: g.IO C
~
~
I
Ma~ I
I
I
JUIll: I
I
I
July I
I
I
Aug. I
I
I Sept. I I I
Oct. I
I
I
I
ov. I
l.LJ
Fig. 3. Sporophore production by Coprinus plicatilis in 1964, in relation to rainfall and average soil temperatures at 10 cm depth; by ro-day periods. The dates and intensities of the first air frosts of the season are also indicated.
COVER CROP AND FERTILIZER EFFECTS
Numbers of sporophores The major cover-crop effects are summarized in Table 4. In general (and within the limits of the statistical analysis imposed by the changed scope of the experiment from 1967 onwards), the results show that Panaeolina foenisecii and Conoeybe tenera produced the most sporophores on the wild white clover (W) and 'tumble-down' (Z) swards and that Conoeybe
412
Transactions British Mycological Society Table 4, Mean numbers of sphorophoresfplot, in relation to sward
(W, Wild white clover; Z, 'Tumble-down'; X, Perennial ryegrass; T, Timothy grass,) Swards --'
W All species
1964 1965 1966 1967* 1968* 1964-8*
22'6 39'6 62'1 (0'5 (46'2 (175'4
1964 1965 1966 1967* 1968* 1964-8*
19'1 35'3 55'4 (0'5 (46 '0 (159'4
1963 1964 1965 1966 196 7* 1968* 1963-8*
0'2 1'0 1'9 2'0
I
Panaeolina joenisecii
Conocybe lactea
Coprinus pluatilis
Conocybe tenera
1963 1964 1965 1966 1967* 1968* 1963-8* 1964 1965 1966 196 7* 1968* 1964-8*
Z 17'2 4 2'3 36 '4 1,8) 12'0) 123'0)
X
6'2 26'4 31"6 (2'4 (25'0 lIOS,8 1,6 12'1 34'8 15'4 28'1 22'8 (0,8 -) 10,8) (20'1 98'6) (75'5 1,8 6'1 1,6 2'1 5,8 3'3 4,8 1'7
-)
T 10,8 20'5 27'2 0,6) 24'5) 90'0)
1'3 10,6 20'9 0'1) 23'6) 65'4) 0'5 2'0 3'9 1'4
0'1 0'3
0'3 1'6 0'3 0'3
(0'1 (21'0 1,6 0,8 0'9 1'1
7'2} 6-6 5'2 0'9
(0'1 (0'5
0'9) 3,8)
(0'2 (6'1
0'2) 19'5)
0'9 0,8 4'0
0'2 1'0 5,6 0'1) 0'1) 7'4)
1'4 (0'1 (0,6 (1,6
0'5 0'7 3'2 0'2) 0'2) 4'1)
(0'1 (8,6 0'3
(-
(-
(6,8
9'4)
Significant differences
(W> X, T, Z-nearly 5%)
W> X, T(5%) W, Z > T(5%) (W> X, T, Z-nearly 5%) (W, Z) > (X, T) (5 %)
X> W(I%); > Z(5%) X> W, T, Z (I %)
0'1) 6,6) T> W, Z, X(I%) T> W, Z, X (0'1 %)
(X, T) > (W, Z) (I %) W,Z>X(5%) Z> X, T(I%) (W, Z) > (X, T) (I %)
* These data are for the 32 C untreated' plots only, for which the only valid comparison is between pI of treatments- (W, Z) v, (X, T),
lactea did so on the perennial rye grass (X) sward and Coprinus plicatilis on the timothy grass (Y), The only noteworthy fertilizer effects (Table 5) were that fruiting in Conocybe tenera was significantly depressed by added superphosphate (P) and that in P.foenisecii it appeared to be depressed by both Nitro-chalk (N) and sulphate of potash (K), although it was only for the last that the level of significance approached 5 %. Specific frequencies and distribution Sporophore production as affected by the different treatments is a function of the number and extent of the mycelia present in the soil of the plots concerned as well as of their individual fruiting capacity, Whilst there is no information available on the extent of the individual mycelia,
Productivity of macro-jungi. T. E. T. Bond Table 5. Mean numbers of sporophores/plot, in relation to fertilizers Fertilizers Significant differences
\
N
Panaeolina foenisecii
1964 1965 1966 196 7* 1968* 1964-8* Corwcybe tenera 1964 1965 1966 1967* 1968* 1964-8*
6,8 22'5 3°'3 0'4 23'5 87'4 0'5 0'7 3,8 0'2 0'4 5'4
NoN 10'2 25'5 33'3 0'2 26,8 II2'j 0'3 0'5 3'2 0'1 0'1 4,6
P
NoP
K
NoK
10'2 27.8 34'2 0'1 21'3 96 '8 0'2 0'2 2'4 0'1 0'2 2'9
6,8 20'3 29'3 0,6 28'9 102'6 0,6 1'0 4'7 0'1 0'2 7'1
7,8 19'4 3 1'0 0'4 16'3 73'7 0'2 0,6 3'9 0'1 0'1 5'0
9'2 28·6 32'6 0'2 33'9 12 5'8 0'5 0,6 3'2 0'2 0'4 4'9
} No P > P (5%) No P > P (5%)
* These data are for 32 'untreated' plots only; the remainder for all 64 plots,
Table 6. Specific frequencies per plot in relation to sward andfertilizer treatments, 1964-8 ( 'Expected' values in parentheses) In whole experiment In relation to treatments
Corwcybe /actea C. tenera
47/64 48/64
Coprinus plicatilis C, lagopus
43/64 19/64
W Wild white clover sward. X Perennial ryegrass sward T Timothy grass sward.
X: 13 (II'75)/16 W, Z: 27 (24)/32 No P: 28 (24)/32 X, T: 28 (21'5)/32 W: 0 (4'75)/16
W, Z, T: 34 (35'25)/48 X, T: 21 (24)/32 P: 20 (24)/32
Z,
W, Z: 15 (21'5)/32 X, T: 19 (14'25)/48
Z 'Tumble-down' sward. P With superphosphate. No P Without superphosphate.
an indication of the overall distribution of the several species among the different swards and fertilizer treatments is given by the distribution of the plots from which their sporophores were recorded. The species which it is appropriate to examine from this point of view exclude Panaeolina foenisecii, with a specific frequency per plot of virtually 100 %, and the 'sporadics', of which the occurrence is anyway likely to be at random; which leaves the four species Conocybe lactea, C, tenera, Coprinus plicatilis and C. lagopus, For each of these the null hypothesis of random distribution was examined by X2 test of the differences between the observed and expected plot frequencies for the appropriate sward or fertilizer treatments, as summarized in Table 6. None of the observed differences attained significance at the 5 % level. The number and distribution of the plots occupied by the several species will in turn affect the number of species likely to occur on a given plot. The cumulative total species/plot, 1964-8, ranged from two to seven, with an overall average of 4'3 (c£ Table 2).
Transactions British Mycological Society Times offruiting The predominant influence of weather conditions on the season of fruiting of the fungi is well known and has been demonstrated above for this particular experiment; and it is obvious that any alteration in the normal time of fruiting of a species must depend upon the prevailing conditions for its expression. Ideally, therefore, the records for each year should be examined separately, for each species; but this is quite impracticable on account of the small numbers involved and the relatively high proportion of blanks. Even in the peak year, 1966, there were as many as four plots in which even Panaeolinafoenisecii failed to appear. With these considerations in mind, a detailed analysis was undertaken only for P. foenisecii. The results showed that on the wild white clover (W) and 'tumble-down' (Z) swards, where sporophores were produced in greater abundance than on the other two (see Table 4), the mid-date of fruiting was also advanced - significantly so in 1964 and 1965, by an average of 9'4 and 7'4 days respectively. There were no significant fertilizer effects. DISCUSSION
Most studies of grassland fungi in the past have been made on seminatural swards of long standing, more or less maintained by the grazing animal. Compared with the old permanent pastures, parklands and heaths with which Wilkins & Patrick (1939, 1940) were concerned, for example, the swards studied here have been of far more recent establishment and comprised far fewer plant species. Not only has there been no grazing but there has been frequent passage of machinery for mowing and orchard spraying, with, of course, the complication of exposure to fungicidalspray drift. Of the 70 or so species of fungi which Wilkins & Patrick recorded from their grassland stations on 'clay' (which appear vegetationally to be closer than the others to the present swards) some 10 % were coprophilous and hence would not have been expected in the orchards. Conspicuously absent from among the remainder were Marasmius oreades, Tricholoma gambosum, and species of Clavaria, Entoloma and Hygrophorus, and, in all, fewer than half of the probable species among those listed by these authors occurred. The relative paucity in species of the fungal community here described is perhaps not entirely unexpected; more noteworthy is its strikingly aestival aspect and the preponderance of the single species, Panaeolina foenisecii. The second most abundant species, Conocybe lactea, is one which fails to qualify as a 'constant' in Wilkins & Patrick's lists and is uncommon and absent for many years at a time, according to Holden (1968), at Rothamsted. Also summer fruiting, its relative constancy and abundance in different parts of the country might well be examined in relation to early summer rainfall and other climatic factors. The observed effects of the different swards and fertilizer treatments, though slight, open up a number of possible lines of further inquiry; but they need to be supplemented by information on soil moisture and organic-matter content and perhaps on the micro-climatic conditions within the different swards.
Productivity of macr01ungi. T. F. T. Bond
415
Studies on the effects of fertilizers on fungal fruit body formation (Hora, 1959; Watling, 1965) have been very few. Any detailed investigation of a macro-fungal community is subject to difficulties and uncertainties in recording and to this the present work has been no exception. Chief among these difficulties are lack of information as to the behaviour of the individual mycelia, the small size and relatively short duration of the sporophores of so many species and, in any case, the apparently extreme dependence of fruiting on the concurrence of favourable atmospheric and soil (or other substrate) conditions. While it may be conceded, with Lange (1948), that it 'is clear that every mycelium does not fructify every year', it cannot be assumed that fruiting, when it occurs, is invariably observed. Lange noted that the duration of the fruit bodies of some of the smaller species of Coprinus, Mycena and other genera may be of the order of a few days, or even hours; and, more recently, Richardson (1970) has shown the need for' almost continuous observation of an area if the total sporophore production over a period is to be recorded'. With an interval ofapproximately 10 days between successive observations, as in the present study, it seems likely that the productivity of such species as Coprinus plicatilis and C. lagopus may have been underestimated, but even so it is doubtful whether any of the' constants' for this community have been missed. That there are more 'sporadics' still to be recorded from these swards is virtually certain and there seems no reason to suppose that, among their number, there will not be some that, given a sufficient period of years, might eventually increase to the level of 'constants'. But this is not likely to be realized within the span of 30 years or so, which is the expected life-time of this particular type of commercial apple orchard. I am grateful to Dr C. Bould and Mr R. M. Jarrett, who were responsible for laying out the original field experiment, for their encouragement and for the supply of field-record sheets; to Mr G. E. Clothier and Miss J. Adam (Mrs Campbell) for the meteorological records; to Mr G. M. Clarke and Mr C. R. Baines and staff of the Statistics Section for the statistical analyses; and to Mr R. W. Marsh for kindly reading the manuscript. REFERENCES
BOULD, C. & JARRETT, R. M. (1962). The effect of cover crops and NPK fertilizers on growth, crop yield and leaf nutrient status of young dessert apple trees. Journa of Horticultural Science 37, 58-82. COPE, D. W. (1970). Soil survey of Long Ashton Research Station. Long Ashton Research Station Reportfor 1969, pp. 170-184. DENNIS, R. W. G., ORTON, P. D. & HORA, F. B. (1960). New check list of British agarics and boleti. Transactions of the British Mycological Society 43 (Suppl.), 1-225. HOLDEN, M. (1968). The larger fungi of Rothamsted. Bulletin of the British Mycological Society 2, Ill-1I8. HORA, J. B. (1959). Presidential address: Quantitative experiments on toadstool production in woods. Transactions of the British Mycological Society 42, 1-14. KUHNER, R. & ROMAGNESI, H. (1953). Flore anaiytique des champignons supirieurs. Paris. LANGE, M. (1948). The agarics of Maglemose. Dansk botanisk Arkiv 13, 1-141. RICHARDSON, M.J. (1970). Studies on Russula emetica and other agarics in a Scots pine plantation. Transactions of the British Mycological Society 55, 217-229.
Transcutions British Mycological Society WATLING, R. (1965). Hygrophorus leporinus and its ecology. The Naturalist, Hull, no. 8g3, pp.60-62. WaKINs, W. H. & PATRICK, S. H. M. (1939). The ecology of the larger fungi. III. Constancy and frequency of grassland species with special reference to soil types. Annals of applied Biology 26, 25-46. WaKINS, W. H. & PATRICK, S. H. M. (1940)' The ecology of the larger fungi. IV. The seasonal frequency of grassland fungi with special reference to the influence of environmental factors. Annals of applied Biology 27, 17-34.
(Acceptedfor publication 28 September 1971)
OBSERVATIONS ON THE MACRO-FUNGI OF AN APPLE ORCHARD IN RELATION TO COVER CROPS AND NPK FERTILIZERS By T. E. T. BOND
University
of Bristol, c/o Long Ashton Research Station (With 3 Text-figures)
A study of sporophore production by the higher fungi on experimental apple orchard swards was made on the basis of observations at approximately 10-day intervals during the season, fromJuly 1963 until the end of 1968. In all, some 27 species were recorded, with a total fresh-weight productivity estimated to be ofthe ordet of I - I 0 kg/ha/year. By far the most abundant was the summerfruiting Panaeolinafoenisecii (Pers. ex Fr.) Maire. Productivity and mid-dates of fruiting of this and certain other species were studied in relation to the different types of sward (established from seed in 1955) and to factorial applications of NPK fertilizers, but few significant responses were observed. The records were also exantined in relation to meteorological data as summarized for the early, mid- and late lo-day periods in each month.
The grass orchard sward is a type of semi-permanent artificial grassland which, under modern conditions in this country, is maintained by mowing rather than by the grazing animal. In this respect it may be compared with lawns and other recreational grasslands. There are far fewer species of higher fungi in these vegetational communities than in woodlands or in the more' natural' grasslands and heaths, and their fruiting is in general less conspicuous. Their ecology has been little studied. This paper is an account of 5 (6) years' observations on the higher fungi of a long-standing cover crop and manurial experiment in an apple orchard at Long Ashton. The objectives were to find out what fungi were fruiting in the area, their total and relative abundance and seasonal productivity, their changing behaviour from year to year and their response to the experimental treatments. As will become apparent, the observed effects of the experimental treatments were slight and the results are presented mainly as a record of an intensive survey of the macro-fungal flora of the area in question. THE EXPERIMENTAL ORCHARD
The site and experimental layout were fully described by Bould & Jarrett (1962). The orchard (Nat. Grid ref. ST 534.695) is situated in a shallow E.-W. valley at an altitude of c. 47 m. The soil is a reddish brown imperfectly drained deep loam derived from interbedded Triassic marl and sandstones geologically classifiable as Keuper Marl (Cope, 1970). The site before planting in 1952 had been under continuous arable
404
Transactions British Mycological Society
cultivation for at least 30 years. The planting consists of the three apple varieties: Cox's Orange Pippin, Worcester Pearmain and Bowden's Seedling, planted at 20 ft (6· I m) square with consecutive rows of each variety running from north to south. The trees are all on Malling II stock, and have been trained into delayed open-centre form with a free trunk of about 0·8 m. For the first 3 years after planting the ground was cultivated during the spring and summer, weeds being allowed to grow during the autumn. The cover crops (see below) were sown in April 1955 and the whole area since then has been regularly mown as required, the mowings being left to decompose in situ. During the years under review an area of about 4 m 2 around the base of each trunk has been sprayed with paraquat weedkiller. In addition to the experimental applications of fertilizer, an overall spring dressing of Nitro-chalk has been given yearly. The whole orchard receives a routine commercial spray programme for pest and disease control. The experimental area, a rectangular block of 25 rows of 17 trees, comprises the greater part of the orchard in which it is situated; it covers about Ii hectares (see Fig. I). The four sub-blocks of the layout divide it equally in both directions. Each sub-block comprises four cover crop (main) plots arranged side by side - a full row of 17 trees thus extends over two main plots. For recording purposes, only the even-numbered trees of the varieties Cox and Worcester are used; the third variety, Bowden's Seedling, forms the N.-S. buffer rows. Thus, each main plot consists offour pairs of recorded trees; each pair, buffered on all sides by guard trees, represents a single sub-plot. The experiment involves four cover-crop treatments (swards), with eight fertilizer (NPK factorial) treatments superimposed, the layout being a randomized block design with partially confounded split plots giving fourfold replication of the main (cover crop) plots and eightfold replication of the sub- (fertilizer) plots. The cover crop treatments comprise one natural sward (' tumbledown', not seeded) and three swards established from seed, respectively, of wild white clover (Trifolium repens), perennial ryegrass (Lolium perenne) and timothy grass (Phleum pratense). Despite the use of selected Aberystwyth 'leafy' strains of the two seeded grass species, already by 1960 (Bould & Jarrett, 1962) there had been a considerable levelling out of the initial sward differences as a result of progressive invasion by Agrostis stolonifera and other grasses indigenous to the locality, and of the natural spread of wild white clQver. Now, some IOyearslater,itseems likely that a still greater uniformity of the swards has been reached, although the perennial rye- and timothy-grass plots are still fairly readily identifiable. The fertilizer (sub-plot) treatments are based on annual applications of Nitro-chalk (15 % N), superphosphate (18 % P 20 S) and potassium sulphate (48 % K 20) at 250, 375 and 125 kgjha respectively, these applications being superimposed on the main plots in combination (a), N: P: K :NPK, or (b), NP: NK: PK: Nil. Since 1967 the experiment has been modified to include the comparison between sward cover and a weedfree environment. This has involved applying herbicide (paraquat and simazine), overall, to half of the plots, and has correspondingly reduced the area of sward available for recording the fungi.
Productivity of macro-Jungi. T. E. T. Bond
405
RECORDING THE FUNGI
Numbers and identity offungal sporophores were recorded on the basis ofsingle' plots' defined as the area ofsward surrounding a pair of recorded trees as far as the mid-line between these and the adjacent guard trees (but excluding the area treated with paraquat around the base of each tree). The procedure was to walk up and down between the Cox and Worcester rows, encircling each tree of the recorded pair in an anticlockwise direction, collecting all sporophores from the sward and discarding them across the plot boundaries. The ground was traversed either a whole row at a time, starting at random from either end of the area or working outwards from the middle, or in half rows taking the sub-blocks of the experiment in random order. Recording commenced in July 1963 and was continued until the end of 1968; from 1964 onwards a full survey was made on the average about 18 times a year at approximately lO-day intervals from the middle of May until the end of November. The main work used for identification was that ofKlihner & Romagnesi (1953). In the account which follows the agaric nomenclature is in accordance with the' New Check List . ..' of Dennis, Orton & Hora (1960) : 'treated' plots are those sprayed overall with herbicide in 1967: the four 'cover crop' treatments are designated W (wild white clover), X (perennial rye grass), r (timothy grass) and Z ('tumble-down'). THE MACROFUNGAL FLORA
Specific frequencies and total sporophore production Table I summarizes the records for the full 5-year period, 1964-8. A total of 24 species is included (or 27 species, if the incomplete records for 1963 are taken into account) of which the first five may be regarded as 'constants' for the experimental area (Wilkins & Patrick, 1939), found in at least a quarter of the individual plots and recorded in at least four years out of the five. The remainder, except possibly for Agaricus campestris, may be regarded as the 'sporadic' element. The close correspondence between specific frequency and total sporophore production is noteworthy, as is the overwhelming preponderance of the single species Panaeolina foenisecii. No direct measurements of weight were made at the time of recording, but observations subsequently have indicated that the yearly average fresh weight production represented by the data in the Table is of the order of 1-10 kg/ha.
rear?J recurrence and persistence The high proportion of 'sporadics' in the mycoflora means that the number of species recorded in anyone year is likely to fall considerably short of the total for the area in question. Thus, Table 2 shows that even in the most favourable years the number of species recorded was only some 60 % ofthe 5-yearly total; and, too, the figures suggest that the cumulative total is still subject to increase. Particular interest attaches to certain species of localized distribution
406
Transactz"ons Brz"tz"sh Mycologz"cal Soaety Table
I.
Occurrence offungi, their specific frequency and total sporophore production, 1964-8
A: 32 ('untreated') plots only, for all 5 years; 3937 sporophores (19 spp.). B: All 64 plots, for 3 years; then 32 ('untreated') plots, for 2 years; 6389 sporophores (24 spp.). (A)
(B)
r - -_ _....J>A
PaTUUlolinafoenisecii* Conocybe lactea* C. tenera agg.* Coprinus plicatilis* C. lagopus Agaricus campestris* Agtocybe semwrbicularis* Lepwta aistata* Lycopetdon depressum Bon.* Marasmius graminum* Clitocybe dealbata* Mycena aetites* Agrocybe praecox Galerina cZavata Coprinus friesii Psathyrella atornata Bolbitius vitellinus Eccilia camrina Bovistaplumbea Fr.* Panaeolus ater Mycena sepia* Omphalina velutina (?) Stropharia coronilla Tubaria conspersa (?)
--.,
, r - - - . . AA- - - - - ,
Occurrence (in years out of 5)
Frequency (in plots out of 32)
Total sporophares
Frequency (in plots out of 64)
Total sporophares
5* 4* 5 4* 4* 4* 2* 3* 2* 3* 2* 1*
32 27 23 22
3 19 1 269 160 159 35 34 22 7 5 20
63 47 48 43 19 9 4 10 3 5
493 1 506 302 303 50 47 60 18 7 76
2
7
3
10
I
II
2
14
I I I I 1
I I I I I
10 2 I 1 I
It I 2 I 1
10 2
1 1*
1
I
1
I
I
I
It 1
II
6 3 3 3 2
9 I I I
1*
I
2
3
17 15 7
I
I
2
I
I
I
I
* Recorded also in 1963 (with Agrocybe temulenta, Conocybe plicatella and Coprinus hemerobius). t In 1968 only, i.e. 1/32.
which may afford evidence of persistence from year to year. Notes on four such species are given below, and the occurrence of the first three of these is indicated in diagrammatic fashion in Fig. 1. Agaricus campestris. Recorded on, or just over the boundary of, 16 plots of which 11 were mutually adjacent in the S.E. corner ofthe area. In these 16 plots a total of 38 yearly occurrences was noted in the period 1963-8 inclusive, representing an average constancy/plot of 2'375 years in six, or nearly 40 %. Sporophores were not recorded in any of the plots in 1965 or in 1967; in three plots they were recorded for each of the remaining 4 years, in four plots for 3 years, in five plots for 2 years and in four plots for a single year only. Clitocybe dealbata. Apparently associated with A. campestris; in five plots only, four of them with records of the latter species in the same year as the Clitocybe, one with records of it in the previous year and again in the year following. Coprinus lagopus. Recorded from 19 plots, with a total of 26 yearly occurrences, making an average constancy/plot of 1'37 years in five (27 %); no great evidence ofpersistence on the plots individually, although
Productivity of macro-fungi. T. E. T. Bond
16 14
.. •
J
~
10 ~
0
8
6 4
2-
J
I
4
,
I
• •
.'
0
0
0
0
0
o~
0
0 ,0
J
10
13 Rows
,
0 0
0
0
7
, ,
I
I
0
I
I
I
• V • •
12
b
.1 IyV V
I
,
16
•
6
0 , ,0
I
,
I-
25
19
I
50m
Fig. I. Sketch plan of experimental area with position of individual plots, showing occurrence of Agaricus campestris (e), Clitocybe dealbata (f) and Coprinus lagopus (0).
Table 2. Numbers oj species ojfungi recorded, Ig63-8 (Cumulative totals in parentheses. A: 32 ('untreated') plots only, 1964-8. B: All 64 plots, 1964-6. C: As 'B', with the preliminary data from July 1963.) B A 1963 1964 196 5 1966 196 7 1968
8 (8)
12 (12)
II (12) II (16)
14 (17) 13 (22)
5 (17) 9 (19) Total recorded area, 64 plots - 0·43 ha.
the marked westerly distribution in the area as a whole (Fig. I) has still to be accounted for. Marasmius graminum. This little (epiphyllous) species was recorded from five plots only; in one of them for 2 years running and in one for two years with a gap of a year between them.
Times ojfruiting Subdividing the fruiting season into lo-day periods ending 20,30 May, gJune, ...,6, 16 and 26 November allowed for the records of sporophore M YC
58
Transactions British Mycological Society I ~'J; I Jilin: I 'II'" I ~1I~. I .' 'p:. I :XII
40 8
\'
t (~ \ II.) .
PI/I/(I('o!il/I/
/f1('II/\ecii
I/prtl/II 11/fl,°PIII
t~ t [
-
(13.
']
\'11.)
Clllwnh(' lI/c/('/1
C.ll!l/l!ra
-
=
(2 . \ III.) Copriml\ p!icuttli
Al!aricll~ F C(lII/Pl·.
lri~
E
.(.. (30.
\'III )
-
Fig. 2. Numbers ofsporophores in lo-day periods, 1964-8, as percentages of the total, with mid-dates offruiting.
production to be reassembled under 'early', 'mid-' and 'late' IO-day periods in each calendar month. This was done, for the population as a whole and for the six principal species, as shown in Fig. 2. The mid-dates offruiting are also given, determined from the average intervals to fruiting in days from May 20 as the starting-point (Richardson, 1970). The overwhelmingly aestival aspect of this particular macrofungal population
Productivity of macro-fungi. T. E. T. Bond
409
is indicated by the occurrence, in each of the 5 years 1964-8, of at least 90 % of the total sporophores during the period from late May to late August inclusive; or, in the 5 years together, ofjust over 95 % of the total from early June to mid-August inclusive. This of course reflects the preponderance of Panaeolina foenisecii (77 % of the total sporophores), with its mid-date of fruiting falling between early June (in 1964) and early July (1968), but even so it should be noted that for none of the other principal species does the mid-date of fruiting occur later than the end of August. The two species with the most extended fruiting season are Conocybe tenera and Coprinus plicatilis; in 1964 there was a pronounced 'flush' of the delicate sporophores of the Coprinus during mild weather in late November (see below).
Annual variation Annual variation in the number of sporophores recorded for the principal species is shown in Table 3. An attempt was made to interpret the yearly and seasonal differences in productivity in terms of meteorological factors of which the most significant appeared likely to be rainfall, maximum and minimum air temperature, relative humidity, temperature of the soil at IO cm depth and date of the first autumn frosts. For this purpose the Research Station's meteorological data for each of the 5 years were averaged over lo-day periods and a close visual comparison made with the fruiting records for the same periods (see above). The year 1967, in which the normally most abundant species scarcely fruited at all, was immediately identifiable meteorologically as having the lowest summer (June-August) rainfall of the years in question and the highest autumn (September-November) rainfall. In the summer of that year there was complete drought in both early and mid-June and virtual drought (1'75 mm rain) in earlyJuly and again (0'25 mm) in late August; during the autumn there was exceptionally heavy rain in each of the five consecutive IO-day periods from late September onwards. It is suggested that the predominant summer-fruiting species were largely prevented from fruiting by drought and that some of the more delicate sporophores of such later species as Conocybe tenera and Coprinus plicatilis may have been missed due to mechanical damage caused by the heavy rain or to concealment by the excessive growth of the herbage. For the other 4 years only some very tentative relationships are suggested, as indicated below under the several species: Panaeolina foenisecii. In the peak year, 1966, fruiting was not only exceedingly prolific but it was also unusually concentrated, with 91 % of the total sporophores collected being gathered on two occasions a week apart, in late June. Rainfall during May, June and July of that year was about average, and well distributed, but the soil temperature and maximum air temperature for early June, the minimum air temperature for mid-June and the relative humidities for mid- and late June were all the highest for their respective IO-day periods in any of the years in question. Conceivably, conditions for fruiting of P. foenisecii were so exceptionally favourable that year during June that the fruiting potential of the majority of the mycelia in the soil was exhausted in producing a single exceptionally 29-2
4 10
Transactions British Mycological Society Table 3. Yearly production of sporophores by principal species (Thirty-two plots for 5 years, 1964-8)
Panaeolina foenisecii (mid-date of fruiting) Conocybe lactea (mid-date of fruiting) Conocybe tenera Coprinus plicatilis C. lagopus Agaricus campestris All species
1964 200 (13. vi) 53 (19. vii) 15 66 8 21 37 1
1965 848 (26. vi) 115 (17. vii) 19 56 10 1061
1966
196 7
1328 (27. vi) 98 (4. vii) 114 25 14 5 1601
II
(3. viii) 4 6 42
1968 804 (2. vii) 3 (26. vi) 8 12 3 2 862
large flush ofsporophores towards the end of that month. In 1964 fruiting may possibly have been hastened by the occurrence of above-average soil temperatures for each of the IO-day periods in May and then curtailed by a period of drought in late June; in 1968, it may have been delayed by inadequate rainfall in the early and mid-June periods. Conorybe lactea. The high yield in 1965 was mainly concentrated in a single flush with its peak, in mid-July, following a peak in rainfall of about a month earlier. No such relationship was apparent in 1966. In 1968 there was exceptionally heavy rain (130 mm in 24 h) in mid-July and the only sporophores recorded during the year were a few early ones from the two previous periods. C. tenera. The peak yield in 1966 occurred in three quite distinct flushes, in mid- and late May, in early and mid-August and in mid- and late October respectively. No similar periodicity was apparent in the meteorological data. Coprinus plicatilis. The 1964 season was unusually prolonged, with the last collection of sporophores on 19 November. In that year the pattern of fruiting, with apparently six distinct flush periods, followed closely the pattern of rainfall. The prolonged autumn season was associated with the virtual absence of frost until 30 November and with the occurrence, in both mid- and late November, of above-average air maximum and minimum temperatures and soil temperatures (Fig. 3). C. lagopus. In 1968, these very delicate rather ephemeral sporophores may have been under-recorded following the torrential rain in mid-July (see above). Agaricus campestris. The high yield in 1964 occurred mainly between mid-August and late September. In that year, the soil temperatures and maximum air temperatures for late July and early August were the highest for any of the years in question, as were the maximum air temperatures throughout September, and the rainfall from July onwards, though below average in amount, was well distributed.
Productivity of macro-fungi. T. E. T. Bond
20
6:T E .
.--'--
80
15
/'-..
~l o (/)
.--'-
/
../
"'. "'-
._.""",
13. x.
II. xi. 30. xi.
\~-j~
10
70
411
1 1
60
IE ~ -
50 90 40
~'()
•
~O
60
30
50 40
I
110 G~O
<:
E
~
~ r,;:<: g.IO C
~
~
I
Ma~ I
I
I
JUIll: I
I
I
July I
I
I
Aug. I
I
I Sept. I I I
Oct. I
I
I
I
ov. I
l.LJ
Fig. 3. Sporophore production by Coprinus plicatilis in 1964, in relation to rainfall and average soil temperatures at 10 cm depth; by ro-day periods. The dates and intensities of the first air frosts of the season are also indicated.
COVER CROP AND FERTILIZER EFFECTS
Numbers of sporophores The major cover-crop effects are summarized in Table 4. In general (and within the limits of the statistical analysis imposed by the changed scope of the experiment from 1967 onwards), the results show that Panaeolina foenisecii and Conoeybe tenera produced the most sporophores on the wild white clover (W) and 'tumble-down' (Z) swards and that Conoeybe
412
Transactions British Mycological Society Table 4, Mean numbers of sphorophoresfplot, in relation to sward
(W, Wild white clover; Z, 'Tumble-down'; X, Perennial ryegrass; T, Timothy grass,) Swards --'
W All species
1964 1965 1966 1967* 1968* 1964-8*
22'6 39'6 62'1 (0'5 (46'2 (175'4
1964 1965 1966 1967* 1968* 1964-8*
19'1 35'3 55'4 (0'5 (46 '0 (159'4
1963 1964 1965 1966 196 7* 1968* 1963-8*
0'2 1'0 1'9 2'0
I
Panaeolina joenisecii
Conocybe lactea
Coprinus pluatilis
Conocybe tenera
1963 1964 1965 1966 1967* 1968* 1963-8* 1964 1965 1966 196 7* 1968* 1964-8*
Z 17'2 4 2'3 36 '4 1,8) 12'0) 123'0)
X
6'2 26'4 31"6 (2'4 (25'0 lIOS,8 1,6 12'1 34'8 15'4 28'1 22'8 (0,8 -) 10,8) (20'1 98'6) (75'5 1,8 6'1 1,6 2'1 5,8 3'3 4,8 1'7
-)
T 10,8 20'5 27'2 0,6) 24'5) 90'0)
1'3 10,6 20'9 0'1) 23'6) 65'4) 0'5 2'0 3'9 1'4
0'1 0'3
0'3 1'6 0'3 0'3
(0'1 (21'0 1,6 0,8 0'9 1'1
7'2} 6-6 5'2 0'9
(0'1 (0'5
0'9) 3,8)
(0'2 (6'1
0'2) 19'5)
0'9 0,8 4'0
0'2 1'0 5,6 0'1) 0'1) 7'4)
1'4 (0'1 (0,6 (1,6
0'5 0'7 3'2 0'2) 0'2) 4'1)
(0'1 (8,6 0'3
(-
(-
(6,8
9'4)
Significant differences
(W> X, T, Z-nearly 5%)
W> X, T(5%) W, Z > T(5%) (W> X, T, Z-nearly 5%) (W, Z) > (X, T) (5 %)
X> W(I%); > Z(5%) X> W, T, Z (I %)
0'1) 6,6) T> W, Z, X(I%) T> W, Z, X (0'1 %)
(X, T) > (W, Z) (I %) W,Z>X(5%) Z> X, T(I%) (W, Z) > (X, T) (I %)
* These data are for the 32 C untreated' plots only, for which the only valid comparison is between pI of treatments- (W, Z) v, (X, T),
lactea did so on the perennial rye grass (X) sward and Coprinus plicatilis on the timothy grass (Y), The only noteworthy fertilizer effects (Table 5) were that fruiting in Conocybe tenera was significantly depressed by added superphosphate (P) and that in P.foenisecii it appeared to be depressed by both Nitro-chalk (N) and sulphate of potash (K), although it was only for the last that the level of significance approached 5 %. Specific frequencies and distribution Sporophore production as affected by the different treatments is a function of the number and extent of the mycelia present in the soil of the plots concerned as well as of their individual fruiting capacity, Whilst there is no information available on the extent of the individual mycelia,
Productivity of macro-jungi. T. E. T. Bond Table 5. Mean numbers of sporophores/plot, in relation to fertilizers Fertilizers Significant differences
\
N
Panaeolina foenisecii
1964 1965 1966 196 7* 1968* 1964-8* Corwcybe tenera 1964 1965 1966 1967* 1968* 1964-8*
6,8 22'5 3°'3 0'4 23'5 87'4 0'5 0'7 3,8 0'2 0'4 5'4
NoN 10'2 25'5 33'3 0'2 26,8 II2'j 0'3 0'5 3'2 0'1 0'1 4,6
P
NoP
K
NoK
10'2 27.8 34'2 0'1 21'3 96 '8 0'2 0'2 2'4 0'1 0'2 2'9
6,8 20'3 29'3 0,6 28'9 102'6 0,6 1'0 4'7 0'1 0'2 7'1
7,8 19'4 3 1'0 0'4 16'3 73'7 0'2 0,6 3'9 0'1 0'1 5'0
9'2 28·6 32'6 0'2 33'9 12 5'8 0'5 0,6 3'2 0'2 0'4 4'9
} No P > P (5%) No P > P (5%)
* These data are for 32 'untreated' plots only; the remainder for all 64 plots,
Table 6. Specific frequencies per plot in relation to sward andfertilizer treatments, 1964-8 ( 'Expected' values in parentheses) In whole experiment In relation to treatments
Corwcybe /actea C. tenera
47/64 48/64
Coprinus plicatilis C, lagopus
43/64 19/64
W Wild white clover sward. X Perennial ryegrass sward T Timothy grass sward.
X: 13 (II'75)/16 W, Z: 27 (24)/32 No P: 28 (24)/32 X, T: 28 (21'5)/32 W: 0 (4'75)/16
W, Z, T: 34 (35'25)/48 X, T: 21 (24)/32 P: 20 (24)/32
Z,
W, Z: 15 (21'5)/32 X, T: 19 (14'25)/48
Z 'Tumble-down' sward. P With superphosphate. No P Without superphosphate.
an indication of the overall distribution of the several species among the different swards and fertilizer treatments is given by the distribution of the plots from which their sporophores were recorded. The species which it is appropriate to examine from this point of view exclude Panaeolina foenisecii, with a specific frequency per plot of virtually 100 %, and the 'sporadics', of which the occurrence is anyway likely to be at random; which leaves the four species Conocybe lactea, C, tenera, Coprinus plicatilis and C. lagopus, For each of these the null hypothesis of random distribution was examined by X2 test of the differences between the observed and expected plot frequencies for the appropriate sward or fertilizer treatments, as summarized in Table 6. None of the observed differences attained significance at the 5 % level. The number and distribution of the plots occupied by the several species will in turn affect the number of species likely to occur on a given plot. The cumulative total species/plot, 1964-8, ranged from two to seven, with an overall average of 4'3 (c£ Table 2).
Transactions British Mycological Society Times offruiting The predominant influence of weather conditions on the season of fruiting of the fungi is well known and has been demonstrated above for this particular experiment; and it is obvious that any alteration in the normal time of fruiting of a species must depend upon the prevailing conditions for its expression. Ideally, therefore, the records for each year should be examined separately, for each species; but this is quite impracticable on account of the small numbers involved and the relatively high proportion of blanks. Even in the peak year, 1966, there were as many as four plots in which even Panaeolinafoenisecii failed to appear. With these considerations in mind, a detailed analysis was undertaken only for P. foenisecii. The results showed that on the wild white clover (W) and 'tumble-down' (Z) swards, where sporophores were produced in greater abundance than on the other two (see Table 4), the mid-date of fruiting was also advanced - significantly so in 1964 and 1965, by an average of 9'4 and 7'4 days respectively. There were no significant fertilizer effects. DISCUSSION
Most studies of grassland fungi in the past have been made on seminatural swards of long standing, more or less maintained by the grazing animal. Compared with the old permanent pastures, parklands and heaths with which Wilkins & Patrick (1939, 1940) were concerned, for example, the swards studied here have been of far more recent establishment and comprised far fewer plant species. Not only has there been no grazing but there has been frequent passage of machinery for mowing and orchard spraying, with, of course, the complication of exposure to fungicidalspray drift. Of the 70 or so species of fungi which Wilkins & Patrick recorded from their grassland stations on 'clay' (which appear vegetationally to be closer than the others to the present swards) some 10 % were coprophilous and hence would not have been expected in the orchards. Conspicuously absent from among the remainder were Marasmius oreades, Tricholoma gambosum, and species of Clavaria, Entoloma and Hygrophorus, and, in all, fewer than half of the probable species among those listed by these authors occurred. The relative paucity in species of the fungal community here described is perhaps not entirely unexpected; more noteworthy is its strikingly aestival aspect and the preponderance of the single species, Panaeolina foenisecii. The second most abundant species, Conocybe lactea, is one which fails to qualify as a 'constant' in Wilkins & Patrick's lists and is uncommon and absent for many years at a time, according to Holden (1968), at Rothamsted. Also summer fruiting, its relative constancy and abundance in different parts of the country might well be examined in relation to early summer rainfall and other climatic factors. The observed effects of the different swards and fertilizer treatments, though slight, open up a number of possible lines of further inquiry; but they need to be supplemented by information on soil moisture and organic-matter content and perhaps on the micro-climatic conditions within the different swards.
Productivity of macr01ungi. T. F. T. Bond
415
Studies on the effects of fertilizers on fungal fruit body formation (Hora, 1959; Watling, 1965) have been very few. Any detailed investigation of a macro-fungal community is subject to difficulties and uncertainties in recording and to this the present work has been no exception. Chief among these difficulties are lack of information as to the behaviour of the individual mycelia, the small size and relatively short duration of the sporophores of so many species and, in any case, the apparently extreme dependence of fruiting on the concurrence of favourable atmospheric and soil (or other substrate) conditions. While it may be conceded, with Lange (1948), that it 'is clear that every mycelium does not fructify every year', it cannot be assumed that fruiting, when it occurs, is invariably observed. Lange noted that the duration of the fruit bodies of some of the smaller species of Coprinus, Mycena and other genera may be of the order of a few days, or even hours; and, more recently, Richardson (1970) has shown the need for' almost continuous observation of an area if the total sporophore production over a period is to be recorded'. With an interval ofapproximately 10 days between successive observations, as in the present study, it seems likely that the productivity of such species as Coprinus plicatilis and C. lagopus may have been underestimated, but even so it is doubtful whether any of the' constants' for this community have been missed. That there are more 'sporadics' still to be recorded from these swards is virtually certain and there seems no reason to suppose that, among their number, there will not be some that, given a sufficient period of years, might eventually increase to the level of 'constants'. But this is not likely to be realized within the span of 30 years or so, which is the expected life-time of this particular type of commercial apple orchard. I am grateful to Dr C. Bould and Mr R. M. Jarrett, who were responsible for laying out the original field experiment, for their encouragement and for the supply of field-record sheets; to Mr G. E. Clothier and Miss J. Adam (Mrs Campbell) for the meteorological records; to Mr G. M. Clarke and Mr C. R. Baines and staff of the Statistics Section for the statistical analyses; and to Mr R. W. Marsh for kindly reading the manuscript. REFERENCES
BOULD, C. & JARRETT, R. M. (1962). The effect of cover crops and NPK fertilizers on growth, crop yield and leaf nutrient status of young dessert apple trees. Journa of Horticultural Science 37, 58-82. COPE, D. W. (1970). Soil survey of Long Ashton Research Station. Long Ashton Research Station Reportfor 1969, pp. 170-184. DENNIS, R. W. G., ORTON, P. D. & HORA, F. B. (1960). New check list of British agarics and boleti. Transactions of the British Mycological Society 43 (Suppl.), 1-225. HOLDEN, M. (1968). The larger fungi of Rothamsted. Bulletin of the British Mycological Society 2, Ill-1I8. HORA, J. B. (1959). Presidential address: Quantitative experiments on toadstool production in woods. Transactions of the British Mycological Society 42, 1-14. KUHNER, R. & ROMAGNESI, H. (1953). Flore anaiytique des champignons supirieurs. Paris. LANGE, M. (1948). The agarics of Maglemose. Dansk botanisk Arkiv 13, 1-141. RICHARDSON, M.J. (1970). Studies on Russula emetica and other agarics in a Scots pine plantation. Transactions of the British Mycological Society 55, 217-229.
Transcutions British Mycological Society WATLING, R. (1965). Hygrophorus leporinus and its ecology. The Naturalist, Hull, no. 8g3, pp.60-62. WaKINs, W. H. & PATRICK, S. H. M. (1939). The ecology of the larger fungi. III. Constancy and frequency of grassland species with special reference to soil types. Annals of applied Biology 26, 25-46. WaKINS, W. H. & PATRICK, S. H. M. (1940)' The ecology of the larger fungi. IV. The seasonal frequency of grassland fungi with special reference to the influence of environmental factors. Annals of applied Biology 27, 17-34.
(Acceptedfor publication 28 September 1971)