The annual cycle in populations of earthworms (Lumbricidae, Oligochaeta) in three types of oak-hornbeam of the Niepolomicka forest. III. Energy flow through earthworm populations

8 Pages·1994·1.5 MB·English

by  Jean-François Ponge

Pedobiologia 38, 28-35 ( 1994)
Gustav Fischer Yerlag Jena
The annual cycle in populations of earthworms (Lumbricidae, Oligo
chaeta) in three types of oak-hornbeam of the Niepolomicka Forest.
III. Energy flow through earthworm populations
Anna Rozeo
Institute of Environmental Biology. Department of Ecosystem Studies. Jagiellonian University. ul.
Ingardena 6. PL-30-060. Krakow. Poland
Summary. Earthworm populations were studied in three Yarietes of oak-hornbeam forest
(low. high-moist. and high-dry) at Niepolomice Forest. The data on species composition.
numbers. age structure and their annual \'ariations were used to calculate annual respiration.
production. assimilation and consumption. The earthworm populations of 142.8 ind. · 111-2.
174.7 ind. · m-2, and 65.5 ind. · m-2 in the three forest types had respiration of 255.8 kJ
· m-2 · a-1, 282.2 kJ · m-2 · a-1• and 97.9 kJ · m-2 · a-1 respectively. The production of
the earthworm populations in these varieties of oak-hornbeam forest was I 94.4 kJ · m -2
·a - i. 21 :u kJ · m -2 ·a - i and 78.3 kJ · m -2 ·a - i respectively. The earthworms consumed
about 25% fallen leaves and dead herbaceous vegetation from the forest noor.
Key words: Earthworms. energy now. metabolism, consumption, respiration. production
Introduction
The International Biological Programme helped to formulate basic rules governing the
energy Dow in ecosystems (Grodzinski, Klekowski & Duncan 1975). Niepolomice Forest
near Cracow was one of the study sites of lBP in southern Poland. The research carried
out there concentrated on the functioning of a forest ecosystem under pressure of industrial
emissions (Grodzinski, Weiner & Maycock 1984). These studies did not. however, cover
soil fauna - a compartment of significant importance for energy Oow and matter cycling.
To bridge this gap, the data on species composition, population numbers, biomass. and
age structure of the earthworm fauna in Niepolomice Forest (Rozen 1982, 1988) were used
in the assessment of energy Oow through earthworm populations and of their role in the
ecosystem.
Materials and methods
Study area
The studies were carried out in the northern part of Niepolomice Forest complex (20cl 7' -20°27' E
and 50°4' -50°8' N). The soils of the area can be classified as brown gleyed soils of acid reaction (pH
about 5.0). The main forest type there is an oak-hornbeam ( Tilio-Carpinerum) formation. Three sites
were chosen for this study in three distinct varieties of oak-hornbeam forest: low type ( Tilio-Carpinerum
srad1yeros11111). high and moist type (Tilio-Carpinerum typicum variety with Aegopodiwn podagraria L ).
28 Pedobiologia 38 (1994) I
and high dry type (Tilio-Carpi11e111111 typicum variety with Conwllaria maialis L. and Poa 11emoralis L.).
All these stands arc dominated by oak (Querrns rohur L.J, with considerable admixtures of
hornbeam and linden (Ferchmin & Medwecka-Kornas 1976). The oak-hornbeam forest communities
occupy 1048 h including low-type habitats on 401 h (38.8%), high moist habitats on 468 h (44.6%)
and dry high habitat on 179 hectares (17.I %) (Denisiuk & Medwecka-Kornas 1976).
Earthworms were sampled once every month throughout one year. The sampling method used combined
handsorting and expelling by means of a dilute formalin solution (Zajonc 1970). The earthworms
were washed. lightly blotted on filter paper. weighed. and preserved. Each time the soil temperature
was measured the soil humidity was determined (for further details see Ro:Zen 1982. 1988).
C a/culat ion meth ods
The energy now calculations were based on the following relationship: C = F + U + P + R:
A = P + R where C (consumption) - energy taken in with food. F - energy in faces. U - energy
in urine. P (production) - energy incorporated into animal"s body and used for reproduction. R
(respiration) - energy dissipated (used in life processes). A (assimilation) - the portion of energy
in food that is used to cover energy costs of living activities and production.
The data available included species composition. annual dynamics of changes in population numbers.
biomass and population age structure in the three oak-hornbeam forest sites at Nicpolomice. The set
of data did not include biocnergetic parameters: relevant data from other available sources were used
for these. Data on respiration in various earthworm species are relatively abundant while information
on other bioenergetic parameters is rather patchy. For this reason the calculations \\ere started by
determining respiration.
The body mass of eartll\\ orm' collected in Niepolomic.: Forest included the gut contents comprising
about 25~o of body mass in Ap11rrec111dt•11 caligi11osa (Savigny. 1826). A. rusea (Sadgny. 1826) and
Ou11/11sit111 lac1eu111 (Ocrle). 1881). 18°0 in De11tlrohae1w ocwedrn (S<l\igny. 1826). D. ruhida (Eisen.
1874) and £i.1e11iella Telraedra (S<l\ign). 1826). 16°0 - in L11111hricus ruhellm (Hoffm.:ister. 1843:
Phillipson & Bolton 1976) and 15° o in Fi1:_n1gt'l"i11 pllllyura (Fitzingcr. 1833). Rele\ant corrections
\\ere introduced to exclude gut contents from the bod~ mass data. The indi\ iduals of various specie>
\\ere dh id.:d into adult (ad) and immature specimens (imm) of four \\eight classes \\ith 0.1 g intervals
for .-1. caliginosa . .-1. rosca. 0. /m·1£•11111 and L. ruhe/111.\ or 0.05 g intcnals for D. octacclra. D. ruhitla.
F. plat_rnra and £. 1e1racdra because of their IO\\ number,_ \\cre divid.:d onl~ into adults and immature
individuals. Respiration was computed on the b;isis of the equation describing the rel;itionship bet\\een
the bod~ mass and respiration: R = a · m1 3 "here R - respiration in pi 01 • hr -1• m - bod) mass
in g. The ··a·· coefficient wa~ calculated from e"perimental data a\ailable in the literature (Konopacki
1907: Barley & Jennings 1959: Satchell 1967: Bolton & Phillipson 1976: Phillipson & Bolton 1976:
Phillipson et al. 1978: Fitzpatrick et al. 1987) and had the follo,\ing \alucs: 57 for .-1. caligi1111.rn and
L. ruhellus (al 15 C). 39 for .-1. rn.sea (at 10 CJ. ;ind 52 for D. uctaedra (al 10 C).As data for 0.
lm·1e11111. F. plw_rnra and £. tetraetlra \\ere lacking. data for species resembling them in respect of
habitat and size \\ere used: i.e. the rl. cc1/igi1111sc1 \alue was applied to 0. laL·te11111. the D. 11u11eclra
value was applied to D. ruhitla and £. 1c1raetlra and that available for L. terre:>Tris (63 at 15 C) -
was used for F. plat_rnra.
The soil temperature at "iepolomice Forest ranged from 0 C to 13 C and comersion from th.:
experimental temperatures used in the studies cited to field soil temperatures \\aS based on the following
formul;i (Persson & Lohm 1977): R,. = R, · Q'!o-" 10 \\here: R, - respiration at experimental
temperature. R,m - respiration at temperature required. and the Q \alue "as assumed to be 2.0
10
(Phillipson & Bohon 1976: Fit7patrick et al. 1987). The respiration values \\ere calculated according
to the above procedure for all the species and age groups for all months of the year. An oxycalorific
equivalent of 19.979 J · ml-10 was used to convert O\ygen consumption to energ) equivalents.
1
Production was estimated on the basis of th.: regression equation gi\cn by Humphreys ( 1979):
log P = 0.942 log R - 0.019 where P is production and R is respiration in kcal m -i a - '.The equation
given by Humphreys seems to be the best one based on experimental d<1l<1 obtained for long-living
saprophagic invertebrates. For the sake of comparison. production was also estimated according Lo
McNeill and Lawton·s equation (1970): log P = 0.8233 log R - 0.2367 and from the relationship
between biomass and turno\er (Grodzinski et al. 1966): P = N · m · 0 ·Kb where: N - population
number (m-2 a - 1). m - average body mass of individual (g). 9 - turnover of individuals (ind. ·a - 1).
Kb - calorific value of biom<1ss (kJ · g- 11• The average life span was assumed to be two years (Satchell
1967; Phillipson & Bolton 1977). The calorific equivalent of animals· bodies ( 13.32 kJ · g- 1 dry weight)
was taken from Bohon & Phillipson (1976).
Pcdobiologia 38 ( 1994) I 29
Assimilation was calculated acc6..rding to the formula: A = P + R Experimental measurements of
consumption levels in earthworms are fe\\ and vary considerably which makes it difficult use them
for computations. hence a percentage A C coefficient was used. Bolton & Phillipson ( 1976) give values
of I 0 o for energy and 2.5° o for organic mailer for A. ro.sea. Crossley et al. ( 1971) determined the
coefficient of assimilation for caesium isotope in 0. /acre11111 as 11.6- 28.6%. and for L. rerresrris as
25.4 ± 4.26%. A uniform \'alue for the coefficient of assimilation of 10% was applied to all the
earthworm populations at . "iepolomice Forest. This was by far the weakest point of the computation
procedure which might introduce the largest error.
Results
On the three sites at Niepolomice Forest the following are the estimated mean earthworm
numbers and biomass fowres: low oak-hornbeam rorest - 142.8 ind. · m-2. 32.6 · g m-2.
high moist oak-hornbea~1 forest - 174.7 ind. · m-2• 31.2 g · m- 2• high dry oak-hor~beam
forest - 65.5 ind. · m-2• 14.1 g · m-2.
The respiration figures for particular species and age groups are given in Tables I and 2.
The sites differ in respect of the contribution or species and age groups to total respiration.
In )O\\ oak-hornbeam forest. the largest portion or dissipated energy goe!> through the
0. lacre11111 population and in both high oak-hornbeam forest sites through A. caligi110.rn
(Table 2). In high moist oak-hornbeam forest. the site with the highest earthworm density.
there is a distinct domination of respiration by immature indi' iduals. in the low
oak-hornbeam forest site the adults and immature indi,·iduals contribute to overall
respiration more or less equally. while in the high dry site ,,·hitch had the lowest
densit~ respiration by adult earth,,·orms was predominant. The abo\'e relationships
correspond with the species composition and age structure of the earthworm populations
present ( Rozen 1988). Throughout the year the respiration le\'els nuctuate. reaching
maximum values in spring and summer and minimum in the ''inter months (Fig. I).
Similar relationships were observed in respect to assimilation and consumption levels
(Table 2).
kJ-m-2
10
8
6
4
2
jul sept nov jan mar may
Fig. I. Annual changes in respiration or Ocrolasion /acte11111 and Demlroha£•11a ocraedra (in kJ · m-~).
Symbols: 0---0 - adult individuals of 0. lac1e11111. o o - immature individuals of 0. /ac1c11111.
"-----" - adult indi\iduals of D. ocraedra. ,.. x - immature individuals of D. octaedra
Discussion
The average density of earthworms for the entire oak-hornbeam complex was 143.8 ind.
· m -2 and the average biomass was 28.93 g · m -2. Average respiration was 240.8 kJ
· m -2 ·a - i. production was 182. 7 kJ · m -2 · a - 1• assimilation was 423.6 kJ · m - 2 · a - 1•
and consumption was 4235 kJ · m -2 • a - 1 (Fig. 2).
30 Pedobiologia 38 (1994) I
Table I. Respiration (kJ · m-2 ·a -1) of earthworm species and age classes in Niepolomicka Forest
A. caligi11osa A. rosea 0. lacceum D. ocraedra
ad imm ad imm ad 1mm ad imm
low oak-hornbeam 18.2 10.3 25.3 28.0 49.8 41.5 20.7 12.7
moist high 30.5 74.5 32.8 42.3 12.1 7.0 16.8 13.8
oak-hornbeam
dry high 19.6 19.7 8.7 8.4 3.4 1.2 14.7 8.0
oak-hornbeam
Nore: ad - adult individuals. imm - immature individuals
tree leaves herb layer
8170 :·813
R
dead
roots respiration 241
I? 1
\.
litter I-20401 '\Iii,.., ~-c_co_n _s4u_m2_3p_t5i_o _n___, earthworms production p
183
' ' ' ?. I I I
" I egestion 3781
bacteria. fungi
Fig. 2. Encrg~ no11 through canhworm populations in Nicpolomicka Forcsl (in kJ . Ill-~ . a -I)
The annual leaf production at iepolomice Forest \\"US 81. 71 . I ob kJ . ha - I . a - l ( :Vled
wecka-Kornas et. al. 197..+). and that of the herbaceous ground layer was 8.13 · 106 kJ
·ha - l ·a - l (Rieger et al. 198.+). In all. the energy input into the litter layer was about
90 · 106 kJ · ha - • ·a -•. This does not constitute the entire food supply for earthworms as
they supplement their diet with dead roots. for example. Assuming that they feed exclusively
on fallen leaves and herbaceous litter. they \\"Ould ha\·e been responsible for consuming as
much as 47% of these components.
So far. only a few reports on energy flow through earthworm populations and on energy
budgets for particular earthworm species have been published. Lavelle (197..+) calculated
energy budgets for earthworms of African savanna. Nowak (I 975) estimated earthworm
production on pastures. Bolton & Phillipson (1976) estimated the energy budget of
A. rosea while Phillipson et al. ( 1978) estimated energy flow through the earthworm
population in a beech forest in England.
The calculation of energy flow through the earthworm populations in the oak-hornbeam
forest of Niepolomice was based on estimated numbers and biomass. According to
Pedobiologia 38 (1994) I 31
D. rubida L. r11be/111s F. plar.rnra E. rerrraedra total
ad imm ad imm ad imm ad imm ad imm
1.5 0 4.5 17.7 2.8 9.6 1.0 2.1 123.8 131.0
.5 .3 11.7 38.9 105.3 176.9
1.0 .1 4.7 8.4 51.1 45.8
Grodzinski & French (1983). accurate estimation of these two parameters is of critical
importance. Inaccuracy in subsequent steps of the calculations has much less effect on the
O\ erall estimate of energ) now.
Respiration b) the earthworm population in oak-hornbeam forest \\·as close Lo that reported
b) Phillipson et al. ( 1978) for a beech forest in England (2 I 4. 7 - 268.4 kJ · m -2 · a - 1 ). and
also Lo the \·alue (266. 7 kJ · m -2 ·a-1) reported by :v1acfadyen ( 1963) for another beech
forest. All the abO\e respiration assessments are similar e\·en though the earthworm numbers
at Niepolomice were higher. It seems that the effect of numbers has been offset by
the differences in the biomass of the earthworm population and in soil temperature. In
the English beech forest. large earth\\ orm species such as L. 1erres1ris and A. /01rga
were represented in great numbers while in . iepolomice the only species of this size
r F. plar_rnra; was ·rather rare. In the milder climate of England. the soils are warmer in
winter and spring than are the soils of Niepolomice. with similar temperatures pre\'ailing
in summer. Such a pattern increases respiration because earthworms are acti\'e for
longer.
Earth\\Orm respiration \"a)ucs reported b) rnrious authors can be compared as the) are
experimentally determined or at least computed on the basis of experimental data. The
procedure for calculating production is much more complex and the \'arious methods of
computing it ma) preclude any atlempt to compare data reported b) \arious sources. The
results obtained by the three methods used in the present study differ considerably. A
moderate estimate of production (I 82. 7 kJ · m -i · a - 1) was yielded b) Humphreys· method.
while McNeilrs regression gave almost three times less. and the production biomass
relationship. twice as much as the Humpreys method (Table 3). Humphreys· regression
relates to Jong-living detritophagous animals and was based on experimental data for
earthworms: it was thus considered to be the most appropriate method for calculating
production in the present study.
The consumption estimate for the earthworm population is the most difficult one to
achieve and is the one subject to the largest error. The estimate of almost 47% con
sumption of energy present in fallen leaves from trees and litter is probably too high
as the food supply includes dead roots. soil organic matter. bacteria. fungi. algae and
small soil fauna (Atlavinyte & Pociene 1973: Bouche & Kretschmer 1974: Lee 1985:
Piearce I 972, I 978). A more realistic assumption is that earthworms consume about
25% of annual fall of tree leaves and herbaceous litter (Satchell 1983: Zicsi 1983). Accord
ing to Satchell (I 963). the population of only one species ( L. 1erre.wis) consumed
annually about 8- I 0% of total leaf-fall. while Lee (I 985) calculated the consumption at
about 5%.
The estimate of 25% consumption of fallen leaves and herbaceous vegetation obtained for
the earthworm population in Niepolomice Forest signifies the role of this group of animals
in the acceleration of litter decomposition.
32 Pedobiologia 38 (1994) I
...,
Tahlc 2. Respiration (R), production (P). assimilation(/\) and consumption (C) of earthworms in Nicpolomicka Forest (in k.1·111-2 • a-1)
,f. ca/igino.rn ,f. r11s1•a O. lacte11111 /), OCllll'<fm D. mliida L. ruhe/111.v F. p/aty11ra E. tertraedra total
low oak-hornhcam R 28.5 53.4 91.J JJ.4 1.5 32.3 12.4 3.1 255.8
r 24.5 44.2 7J.J 28.4 1.5 27.5 11.6 3.0 194.4
I\ 5J.0 97.6 IM.6 61.8 J.O 59.8 24.0 6.2 450.2
c
530.3 975.6 1646.0 618.1 29.5 597.5 242.6 62.2 4504.3
moist high R 105.0 75.1 19.1 J0.6 .8 51.6 282.2
oak-hornhcam r 8H1 61.0 I (>.8 26.2 .9 42.8 212.2
I\ IRK.6 IJ6. I J5.8 56.8 1.7 94.4 494.4
c
1885.7 1361.2 358.J 56lU 16.8 944.0 4944.1
dry high R 39J 17.1 4.6 22.7 I.I 13.1 97.8
oak-hornhcam p JJ. I 15.2 4.4 19.7 1.2 11.8 78.2
I\ 72.4 32.J 9.0 42.4 2.J 24.9 176.1
c
724.2 J2J.O 89.5 423.6 22.6 248.9 1761.4
"'d
~
0
0-
£
0
(IQ
.i.i.i,'
QC
'°
.':°=
w
w
Table 3. Production (kJ · m-2 ·a -1) of earthworms in Niepolomicka Forest calculated using three
different methods
Respiration Production
(A) (B) (C)
low oak-hornbeam 255.8 194.4 71.9 370.1
moist, high oak-hornbeam 282.2 212.2 77.9 353.2
dry, high oak-hornbeam 97.9 78.3 32.6 160.1
whole oak-hornbeam stand 240.8 182.7 67.5 326.6
.l\'01e: (A) - Humpreys (1979): (B) - McNeil & Lawton (1970): (C) - Grodzinski et al. (1966)
Acknowledgements
I am grateful to the late Prof. Dr. W. Grodzinski and Lo Dr. J. Phillipson for ad\'ice during the
preparation oft he manuscript. I wish to thank Dr. J. Weiner fon·aluable comments on the manuscript.
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3• Pedobiologia 38 (1994) I 35