Profile by Lumbricus Rubellus Hoffmeister
THE TRANSPORT OF MINERAL AND ORGANIC MATTER INTO THE SOIL
PROFILE BY LUMBRICUS RUBELLUS HOFFMEISTER
by
HUBERT J. TIMMENGA
Landbouwkundig Ingenieur, Wageningen, 1981
A THESIS SUBMITTED IN PARTIAL FULFILMENT OF
THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY
in
Soil Science
THE FACULTY OF GRADUATE STUDIES
Department of Soil Science
We accept this thesis as conforming
to the required standard
THE UNIVERSITY OF BRITISH COLUMBIA
13 September 1987
© HUBERT J. TIMMENGA, 1987
k 6 In presenting this thesis in partial fulfilment of the requirements for an advanced
degree at the University of British Columbia, I agree that the Library shall make it
freely available for reference and study. I further agree that permission for extensive
copying of this thesis for scholarly purposes may be granted by the head of my
department or by his or her representatives. It is understood that copying or
publication of this thesis for financial gain shall not be allowed without my written
permission.
Department of
The University of British Columbia 1956 Main Mall Vancouver, Canada V6T 1Y3
DE-6(3/81) ABSTRACT
The biology and ecology of the earthworm Lumbricus rubellus
Hoffmeister, 1843, and its effects on the turn-over of organic matter and soil are not well known. To gather this information, the ingestion and egestion rates were measured using a litterbag technique and the transport of organic matter was quantified with a newly developed method, using soil columns to which 14C labelled plant material was added.
The feeding habits of the worm were positively influenced by temperature in wet soils (> -15m of water) and were negatively influenced in dry soil (< -15. m of water). The total egestion rate changed from 0.3 g.g-'.day"1 at 5 °C to
1.0 g.g~1.day~1 at 20° C in moist soil (- 5 m of water). The egestion rate at medium range temperatures, 10 and 15° C, was less affected by drought stress than at 5 and 20 °C. The egestion rate of carbon was a more stable parameter than the total egestion rate, and ranged from approximately 20 mg.g-1.day"1 at 5 °C, to 50 mg.g-1.day_1 at 20 °C.
The moisture and temperature effects were apparent in the
Q10 of the total egestion rate and of the egestion rate of
carbon. The Q10 ranged from 1.66 in wet soils to 3.27 in dry
soils in the 5-15 °C interval and from 1.98 to 0.32 in the
10-20 °C range. For the egestion rate of carbon, the Q10
i i ranged from 1.92 to 3.21 and from 1.28 to 0.47, respectively.
The body water content of the worm varied considerably with the soil water potential, and reached a maximum level of 5.5 kg.kg"1 (dwt) between -15 metres of water and -30 metres of water. When under drought stress, worms stopped ingesting large quantities of soil, switched to a diet high in organic matter and lowered their activity.
In the 1"C column experiment, the total cast production was significantly related to depth. L. rubellus produced 15 % of the cast on the surface of the soil, 46 % in the 0-5 cm layer, 22 % in the 5-10 cm layer and 16 % in the 10-15 cm
layer.
Independent calculations from a) the uptake of 1ftC labelled carbon in earthworms, b) removal of litter from the surface and c) 1"C label recovered from cast, showed that the worms
ingested 78-82 % of the offered organic matter as shoot
litter and 18-22 % as root litter. 1"C originating from
shoot and root litter was recovered in casts throughout the profile, indicating that the worms mixed food from all
layers.
iii The total egestion rate found in the column experiment was
5.2 times higher than was found in the litterbag technique under comparable conditions (2.34 vs 0.45 g.g"1.day"1). The egestion rate of carbon was similar in both techniques (37.1 vs. 46.1 mg.g~1.day~ 1 , 10 °C). In preliminary litterbag trials, it was found that L. rubellus egested
15.5 mg.g~1.day~1 of carbon (5 °C) for each of four food types offered. The 5 °C temperature trial of the litterbag technique, showed a similar amount of carbon egested. It was concluded that the worm needed a constant amount of carbon to provide nutrients and energy, of which a part or all may originate from ingested microorganisms.
Based on the distribution of cast in the profile and the feeding strategies of L. rubellus, it was concluded that this earthworm cannot be classified as an epigeic worm. A new strategy class was proposed: eurygeic worms, earthworms living in the litter-soil interface, mixing organic matter into the profile and mineral soil into the litter layer.
Based on the literature and results from the present study, a computer model was developed to simulate the longterm effects of earthworms on an agricultural soil system.
Simulations of the mixing of soil and organic matter in a limited-till agricultural system, showed that earthworms
iv negatively affected the accumulation rate of surface litter and positively affected the organic matter content of the mineral soil. The model can be used to predict the trends in organic matter in soils, important in soil conservation, mine reclamation and reforestation.
v TABLE OF CONTENT
ABSTRACT ii
TABLE OF CONTENT V1
LIST OF TABLES X
LIST OF FIGURES xii
LIST OF ABBREVIATIONS xiii
LIST OF SPECIES NAMES xiv
ACKNOWLEDGEMENTS xv
I. INTRODUCTION 1
II. LITERATURE REVIEW 5 A. THE ROLE OF EARTHWORMS IN THE TURN-OVER OF ORGANIC MATTER AND SOIL 5 1. Ecological strategies and classificaton of earthworms 5 2. Earthworm food 9 3. Impact of earthworms on the soil system 14 a. Effects of earthworms on soil structure and fertility 14 b. Effects of earthworms on infiltrability 14 c. The mixing of organic matter into the profile 15 d. Surface cast production 17 e. Parameters affecting the cast production of earthworms 18 B. LUMBRICUS RUBELLUS HOFFMEISTER, 1843 21 1 . Distribution 21 2. Reproduction 24 3. Food sources and eating habits 24 4. Respiration 25 5. Egestion and soil turn-over 25 6. Ecological classification and strategies 26
III. THE EFFECTS OF SOIL MOISTURE AND SOIL TEMPERATURE ON THE EGESTION AND INGESTION RATES OF LUMBRICUS RUBELLUS HOFFMEI STER 28 A. MATERIALS AND METHODS 28 1 . Introduction 28 2. Site description 28 3. Field data collection 29
vi . 4. Earthworms used in the experiments 30 5. Sample collection 30 6. Litterbag technique 31 7. Water content of the worm 35 8. Chemical analysis 36 9. Calculations and Statistics 36 B. RESULTS AND DISCUSSION 36 1 . Litterbag technique 36 2. Calculations and statistics 37 a. The grouping of the moisture and temperature levels 37 b. Calculation of the ingestion rates 37 c. Statistical analysis 37 d. Curve fitting 39 3. Egestion rates of soil and organic matter 39 4. Egestion rate of carbon 43
5. Q10 values of the activity of earthworms 45 6. Faecal organic matter 47 7. Faecal water content 49 8. Ingestion rates 50 9. Worm size 55 10. Soil temperature and soil moisture in the field 55 11. Comparison of ingestion and egestion rates to literature data 56 12. Drought-survival strategies of Lumbricus rube 11 us 59 a. The water content of earthworms ... 59 b. Feeding behavior of the worm as related to the body water content 63 13. Testing of assumption 67
IV. THE TRANSPORT OF ORGANIC MATTER INTO THE SOIL PROFILE BY LUMBRICUS RUBELLUS 68 A. MATERIALS AND METHODS 68 1 . Introduction 68 2. Animals used in the column experiment 68 3. Soils used in the column experiment .... 69 4. Clover used in the column experiment ... 69 a. Production of clover 69 b. Radiolabelling of clover 70 5. Experimental Set-up 71 6. Experimental design and statistics 73 a. Experimental design 73 b. Statistics 74
vii 7. Sample preparation 74 8. Chemical Analysis 75 B. RESULTS AND DISCUSSION 76 1 . Production of clover 76 1 2. *C02 fumigation of the clover 76 3. Observations on materials and techniques used in the column experiment 77 a. Micro-arthropods in the soil 77 b. Plant material 78 c. Experimental temperature and soil moisture content 78 d. Diffusion method for carbon analysis 79 4. Airflow above the columns 79 5. Soil water potentials in the columns... 80 6. Recovery of 1"C activity from the samples 80 a. Specific activity of the recovered materials 80 b. Total activity of recovered materials 83 c. 14C activity recovered from the bulk soil 83 7. Respiration and decomposition 85 a. Respiration 85 b. Weight loss of clover material .... 88 8. Recovery of casts from the soil columns 89 a. Description of the burrows 89 b. Description of casts 91 9. Distribution of casts 91 10. Egestion rates 93 1 1 . Organic matter 95 a. Distribution of organic carbon in the cast 95 b. 1WC activity in casts as related to depth 97 c. Calculation of the use of added organic matter by the earthworms 98 12. Testing of assumption 100
EARTHWORM SIMULATION MODELS 101 A. SIMULATION MODELS DESCRIBING THE DYNAMICS OF SOIL MIXING BY EARTHWORMS 101 1 . Introduction 101 2. Published earthworm models 101 3. "MIXER", a new conceptual model describing earthworm activity in soil systems 104 a. Introduction 104
viii b. Soil layers in the model 105 c. Population dynamics 105 d. Earthworm food 107 e. Cast production 109 f. Flow-diagram for MIXER 109 B. F-MIXER, A SIMULATION MODEL FOR SOIL MIXING BY EARTHWORMS 111 1. Introduction ., 111 2. A brief description of FORCYTE 113 3. Description of the FORCYTE version of MIXER 114 4. Comparison of F-MIXER to MIXER 116 5. Simulation 118 6. Improvements needed in F-MIXER 124
VI. GENERAL DISCUSSION 126
VII. SUMMARY AND CONCLUSIONS 135
BIBLIOGRAPHY 139
APPENDIX 1. Diagnosis of Lumbricus rubellus 153
APPENDIX 2-A. Diagram of the fumigation set-up 154
APPENDIX 2-B. Diagram of the soil column set-up 155
APPENDIX 2-C. Soil moisture and soil temperature on Westham Island 156
APPENDIX 2-D. The population of L. rubellus on Westham Island 157
APPENDIX 2-E. Retention curve of Crescent series soil. . 158
APPENDIX 3-A. Length of litterbag experiments 159
APPENDIX 3-B. Food choices of L. rubellus 160
APPENDIX 3-C. Size and age of L. rubellus, as related to the egestion rate 162
APPENDIX 4. The egestion rate of A. Chlorotica 165
APPENDIX 5. Turn-over of soil and organic matter calculated from the litterbag technique 167
APPENDIX 6. Detailed description of F-MIXER 170
ix LIST OF TABLES Table Page
Table 1. The range of conditions restricting the distribution of L. rubellus 23
Table 2. F-values for interactions and contrasts; ingestion and egestion rates of L. rubellus 41
Table 3. Egestion rates for L. rubellus, probability of data points being different 42
Table 4. The comparison of the total egestion rate with the egestion rate of carbon for four different temperatures and moisture contents 44
Table 5. The Q10 of L. rubellus, calculated from the egestion rate, for different moisture and temperature ranges 46
Table 6. The percentage of organic matter ingested by L. rubellus, calculated from IOM and ITOT and measured in the faeces 48
Table 7. Ingestion rate for organic matter, probability of data points being different 52
Table 8. Ingestion rate for soil, probabilities of data points being different 54
Table 9. The dry weights of the earthworms used in the experiments 55
Table 10. Some ingestion and egestion rates for temperate and tropical earthworms 57
Table 11. Values of Mann-Whitney U-test, indicating differences in body water content 61
Table 12. The water content of soil and clover straw incubated at 20 °C 66
Table 13. 1"C Activity in air samples measured during fumigation 77
Table 14. Specific 1"C activities of materials recovered from the soil columns 82
Table 15. Total 14C activity recovered from materials in the soil columns 84
x Table 16. F-values for contrasts of total cast, recovered from columns, after incubating earthworms with labelled clover shoot or root material added.
xi LIST OF FIGURES Figure Page
Figure 1. The redistribution of soil and organic matter in the soil profile by earthworms 7
Figure 2. The egestion rate (g.g"1.day"1) of L. rubellus related to the soil temperature and the soil moisture 40
Figure 3. The ingestion rate of organic matter for L. rubel I us 51
Figure 4. The ingestion rate of soil for L. rubellus 53
Figure 5. The body water content of L. rubellus, incubated at different soil moisture potentials (19 °C) .60
Figure 6. The body water content (kg.kg"1, dwt) and the egestion rate (g.g~1.day"1) of adult L. rubellus at 20 °C 65
Figure 7. Pressure potentials in the soil column during the incubation 81
Figure 8. Decrease in1 "C activity (% first
measurement) of C02 released through respiration 86
Figure 9. Distribution of cast ( % of total cast per column) according to depth 94
Figure 10. Distribution of Carbon (% Carbon) in cast according to depth 96
Figure 11. Flow diagram for the earthworm model MIXER. ..110
Figure 12-A. Results of the simulation of F-MIXER, the accumulation of surface litter 121
Figure 12-B. Results of the simulation of F-MIXER, the organic matter content of layer II 121
Figure 12-C. Results of the simulation of F-MIXER, the ingestion of soil 122
Figure 13. Earthworm strategies as perceived from Bouche (1977) with a new class added 132
xii LIST OF ABBREVIATIONS
Upper mineral soil horizon, intermixed with organic matter
Subsoil horizons
Body water content of earthworms (kg.kg-1 dwt)
Choice of food by earthworms, based on food quality disintegrations per minute
Dry weight
Egestion, Egestion rate (g.g-1.day"1 dwt)
Faeces water content of earthworms (kg.kg'1 dwt)
Ingestion, Ingestion rate (g.g- 1 .day 1 dwt)
Ingestion rate of organic matter (g.g - 1 .day 1 dwt)
Ingestion rate of mineral soil (g.g-1.day"1 dwt)
Total ingestion rate (g.q-1.day"1 dwt)
Litter layer on top of mineral soil
Moisture content of the soil
Organic Matter
Site quality in relation to earthworm populations
Temperature
xiii LIST OF SPECIES NAMES
Al I ol obophora caliginosa Savigny A. chlorolica Savigny A. I onga Ude A. nod ur na Evans A. rosea Savigny A. luberculata Eisen Aporreel odea turgida Eisen Cryptodrilus fasti gat us Fletcher Dendrobaena depressa Rosa D. octraedra Savigny D. pi at yura Fitzinger Dichogaster agiIis Omodeo and Vaillaud Eisenia eiseni Lev in sen E. foetida Savigny E. nordenshi oldi Eisen Eiseni el I a letraedra Savigny Lumbricus castaneus Savigny L. festivus Savigny L. rubellus Hoffmeister L. terreslris Linnaeus Millsonia anomal a Omodeo M. I ami i oana Omodeo and Vaillaud Me gas col ex eel mi siae Jamison Microscolex dubius Fletcher Nicodrilus velox Bouche Octolasion I act eum Orley O. tytraeum Savigny Pheretima alexandri Beddard
xiv ACKNOWLEDGEMENT S
I thank my supervisor, Dr. Les Lavkulich, and the members of my committee, Drs. Shannon Berch, Art Bomke, Ken Hall and especially Valin Marshall, for their effort and guidance.
I gratefully acknowledge the assistance of many faculty members at UBC. Dr. Tony Glass (Department of Botany) kindly accommodated my 1"C experiment in his lab and provided technical assistance. Without his help and that of his staff, the second part of my thesis would have been greatly delayed. Dr. Jim Shelford and Mr. Gilles Galzy (Department of Animal Science) allowed me to use their radio-isotope facilities. Dr. George Eaton (Department of Plant Science) helped me with statistical analyses. Dr. Hamish Kimmins and
Mr. Kim Scoullar (Faculty of Forestry) helped me in shaping the computer simulation model to fit FORCYTE and programming the model. Mr. Bernie Von Spindler and Mr. Peter Synadinos
(Soil Science) helped me by discussing and solving equipment problems. Mr. Mike Curran (Department of Soil Science) read and discussed the manuscript and made many helpful suggestions.
I am also grateful to Dr. Alan Carter under whose guidance this work was initiated and for sharing his experience with the litterbag technique. He provided field data on the
xv earthworm population in a field on Westham Island. Mr. Hugh
Reynolds kindly allowed me to use a part of his farm as an experimental plot.
I especially thank my wife, Yme, for her patience and understanding in dealing with my changing moods. Without her
support, it would have been very difficult to finish this di ssertat ion.
xvi I. INTRODUCTION
Soil organisms have many functions in the process of recycling nutrients and the direction of energy flow in the soil. As decomposers and shredders of plant material, they release nutrients to the soil which become available to growing plants (Wallwork, 1970; Richards, 1972). The most visible impacts of soil animals on the soil system result from the activities of the larger animals such as earthworms and millipedes.
Earthworm activity in the field, as will be discussed in the literature review, is generally quantified by the collection of surface casts or by measuring the effects earthworms have on plant production. Because earthworms may cast below the surface of the soil, it is important to study the total cast production of a species and the distribtion of its casts in the profile, before predictions can be made about the role played in the soil system. A few species such as Lumbricus terrestris and Eisenia foetidai have been widely studied, but other species have not been investigated.
The ecology of Lumbricus rubellus Hoffmeister, 1843, a pioneer species (Reynolds, 1976) is reviewed herein. This tScientific names, cited in this thesis are those reported by the authors. Some names will not reflect modern concepts of earthworm nomenclature.
1 INTRODUCTION / 2 earthworm may play an important role in soil management and reclamation as a soil mixer and litter shredder and as a colonizer of young soils.
The objectives of this thesis are:
1. to study the redistribution of organic matter in the
soil by the earthworm L. rubellus:
a. to quantify the moisture and temperature effects on
the egestion and ingestion rates of the worm;
b. to quantify the cast production related to soil
depth;
c. to quantify the ratio of shoot litter to root litter
in the diet of the earthworm;
2. to develop a simulation model to simulate the long-term
change in organic matter content in the soil through
earthworm activity.
The main hypothesis is that L. rubellus is an epigeic worm, as suggested by Bouche (1977), living in the litter layer and feeding and casting in this layer. It is assumed that soil temperature and soil moisture content have no significant influence on the worm activity (e.g. ingestion or egestion rate) and that L. rubellus uses only surface litter and casts only on the surface of the soil. INTRODUCTION / 3
In this thesis the role of L. rubellus in the redistribution of organic and mineral matter in the soil profile will be discussed based on the results of two experiments. In the first experiment, the influence of soil temperature and soil moisture on the activity (e.g. ingestion or egestion rate) of the earthworm was quantified with litterbag experiments.
In the second, the redistribution of organic matter in the soil profile was studied in a newly developed column experiment, using 1WC labelled clover.
Several experiments were conducted before the main litterbag experiment was executed. The results of these preliminary experiments support the arguments presented in this thesis, although they were primarily conducted to refine the litterbag technique.
Although the thesis is concerned with short-term experiments describing egestion and ingestion rates and transport of organic matter, it was felt that a simulation model would provide insight to the long-term effects of earthworms on the soil system. In the last part of the thesis, a conceptual model, MIXER, is developed from literature data.
It is a non-specific, multi-species model, describing the parameters affecting the turn-over of mineral and organic, matter by earthworms. INTRODUCTION / 4
From this conceptual model and from the results found in the experiments, a computer simulation model was developed. This model simulates the movement of soil and organic matter in the soil profile. Although free-standing, this simulation model, F-MIXER, was designed to be included in the ecosystem model FORCYTE (Kimmins, 1986). F-MIXER neither simulates the daily, weekly or monthly growth nor the soil turn-over of a population of earthworms, but describes long-term trends in organic matter in different soil layers, resulting from earthworm activity. Results of a 45 year trend-simulation in an agricultural no-till cropping system are discussed. II. LITERATURE REVIEW
A. THE ROLE OF EARTHWORMS IN THE TURN-OVER OF ORGANIC MATTER
AND SOIL
1. Ecological strategies and classificaton of earthworms
Earthworm activity is visible in the field because of accumulations of cast on the surface. To quantify the role of earthworms in the soil system, it is necessary to categorize the biological and ecological characteristics of the worms and then classify the animals with similar characteristics into groups.
Earthworms have been classified in many different ways: by morphological characteristics, distribution, relation to human activities and ecological strategies. Bouche (1977) proposed the following classification, based on morphological characteristics, for European lumbricids with different ecological strategies:
Epigeic worms: pigmented, small worms, not good burrowers, slow eaters, moderately sensitive to light, have fast maturation rates and are found in environments rich in organic matter. These worms are highly reproductive and survive adverse conditions by producing large amounts of cocoons. They live and feed in the litter layer. Examples of
5 LITERATURE REVIEW / 6
North American earthworms that are recognized as epigeics
include Eisenia foetida and De ndr obaena oclaedra and an
indigenous undescribed species in the genus Arct iost rol us
(Spiers et al. , 1986).
Endogeic worms: nonpigmented burrowers of medium size, sensitive to light. These "worms are soil dwellers and soil eaters. Adverse conditions are survived in a quiescent state. These worms have a limited reproductive capacity, they live and feed in the mineral soil. Aporreclodia turgida and Octolasion tyriaeum are included in the endogeic class
(Shaw and Pawluk, 1986)
Anecic worms: strong, muscular, deep-burrowing pigmented worms, moderately sensitive to light. They are large and
slow growing. These worms have a low reproductive rate and may survive adverse conditions in a real diapause. They are deep burrowers and may feed on the surface. L. terrestris is
included in this class.
Some species do not fall clearly into any one of the categories. The categories should therefore not be seen as
restrictive. Figure 1 shows the flow of materials in the
soil profile as related to the activities of worms of the
three main categories.
The influence of human activities on earthworm distribution
was described by Julin's system of classification, as LITERATURE REVIEW / 7
BC
Figure 1. The redistribution of soil and organic matter in the soil profile by earthworms. Figure drawn from literature data, Ah = soil layer with biological activity, BC = subsoil, L = Litter, > turn-over of soil, - - -> organic matter used as food (after Bouche, 1977). LITERATURE REVIEW / 8 described and modified by Reynolds et al. (1974). In order of increasing dependence on human influences, earthworms were classified as: hemerophobes, hemerodiaphores, hemerophiles and hemerobionts.
The r-selection and K-selection concepts are generally accepted in ecological theory (Lee, 1985; Satchell, 1980).
The terms r- and K-selection originated from the
Verhulst-Pear1 equation
6N/6t = r(1 - N/K)N which relates population, N, over time to the intrinsic rate of natural increase, r, and the carrying capacity, K, of the environment. Two selections were recognized: r-selection, a selection for maximum population growth in uncrowded, unstable environments, and K-selection, a selection for competitive abilities in stable environments.
Satchell (1980) used the strategy concept to describe earthworm survival strategies. The epigeics were classified as r-worms (high reproduction, small, fast growing) and the anecics as K-worms (efficient survival, large worms, low reproduction). The mentioned strategies represent the limits of a continuum and many worm species such as L. rubellus, L. terrestris and AlIolobophora chlorotica show behavior that LITERATURE REVIEW / 9 includes elements of both strategies.
Difficulties may be encountered in placing earthworms in appropriate categories or strategies. To classify earthworm species according to the role they play in the ecosystem, an
indepth study of each species must be done.
2. Earthworm food
As plant litter decomposes, it is invaded by a succession of microorganisms. Parasites permeate senescing tissue; bacteria, fungi, myxobacteria and protozoa, all living on simple carbohydrates, follow. Cellulose and lignin decomposers, mostly fungi, increase in population in later stages of decomposition (Dickinson and Pugh, 1974).
Different earthworm species ingest organic matter in different stages of decomposition. L. rubellus for example,
ingests relatively undecomposed organic matter, while A.
caliginosa feeds on well-decomposed material (Piearce,
1978). The decomposition of plant material, including the breakdown of calcium oxalate that plants contain, by bacteria and actinomycetes has been described by Cromack et al. (1977). They noted high calcium levels in fungal hyphae and in fungal feeding oribatid mites (up to 18 %) and found calcium oxalate decomposing microorganisms, mostly LITERATURE REVIEW / 10 actinomycetes, in the gut of L. rubellus by plating out the gut content. It is not certain from their data whether the microorganisms actually lived in the gut or simply survived the digestive process.
Relatively undecomposed organic matter may contain high levels of calcium oxalate. This substance may be broken down by fungi and act inomycetes and the calcium may. be taken up by these organisms and by earthworms feeding on them. This phenomenum was also reported by Spiers et al., (1986). They found decreasing amounts of calcium oxalate crystals over the length of the gut of Arct i ost rot us spp, and suggested that the calcium oxalate was used by intestinal microorganisms for their energy needs. The calcium was then absorbed by the earthworm and excreted in the gut as calcium carbonate. Earthworms, such as L. rubellus, which feed on not well-decomposed organic matter, have active calcium secreting glands (Piearce, 1972).
Earthworms ingest large quantities of soil and organic matter, but assimilate only a small amount of the carbon ingested (Uvarov, 1982; Bolton and Phillipson, 1976). Baylis et al. (1986) reported on a 32P study in which feeding of several earthworm species, including L. rubellus, on living clover roots was observed. It is not clear from their paper LITERATURE REVIEW / 11 whether the worms actually fed on the roots, or ingested soil from the rhizosphere. The rhizosphere may contain large amounts of microorganisms, feeding on the root exudates. The label might have been transported to the microbes through root exudates.
Satchell (1983) reported that fungi were selectively destroyed and ingested by L. i errest ri s and that algae and protozoa were digested by L. rubellus. Hartenstein et al.
(1981) found that when specimens of Eisenia foetida were fed with horse manure or sewage sludge, both containing large numbers of microorganisms, the worms ingested a smaller amount of food and gained weight significantly faster than control worms, fed with a soil mixture. Live bacteria and
fungi from axenic cultures contributed to a greater weight gain of worms than did dead bacteria (Neuhauser et al., 1980 b). Flack and Hartenstein (1984) reported that E. foetida grew well on three species of protozoa, and 22 species of bacteria. Also, lyophilized microorganisms were successfully used as earthworm food. Grit, however, including sand or ashed loam, was necessary for optimum growth. Heungens
(1969) reported that when a conifer-needle mixture was
treated with fungicides, less decrease in mixture depth was
seen due to earthworm shredding (mainly by Dendrobaena
spp.), than without disinfection. Either the fungicide was LITERATURE REVIEW / 12 extremely toxic to earthworms, or no fungal hyphae were available as earthworm food after the disinfection, causing a decline in earthworm populations.
Lavelle et al. (1983) found that soil with added hydrocarbons, extracted from leaf litter, made good worm
food. The amount of extract added to the soil negatively correlated with the egestion rate of Millsonia anomala,
indicating a possible direct nutritional value of the hydrocarbons. The worms showed a satisfactory growth
response to all levels of hydrocarbons provided. When soils contained low amounts of hydrocarbons, a high level of microbial growth was observed in the gut content, while with high levels, microorganism growth was decreased. Proteins,
oils and carbohydrates caused weight loss in E. foetida when
presented as worm food. This may suggest that simple
hydrocarbons are not suitable as worm food, while easily
digestible materials such as casein are toxic to earthworms
due to the putrefying effects in the gut (Neuhauser et al.,
1980 b). Shaw and Pawluk ( 1 986) found that L. t err estris and
the endogeic worms 0. tyraeum and A turgida equally
increased the number of actinomycetes and bacteria in the
faeces. In L. terrestris faeces, fungi proliferated, while
the endogeic species enriched the soil with cellulose
decomposing bacteria such as Cytophaga. The increase in LITERATURE REVIEW / 13 microbe biomass in the faeces, as described by Parle (1963), may either be caused by the development of cysts and spores, ingested with the organic matter, and stimulated by a favourable environment in the gut, or by the growth and establishment in the gut of a population of microorganisms in a mutualistic relationship with the earthworm as suggested by Shaw and Pawluk (1986).
The evidence that earthworms utilize either dead or living microorganisms as food or utilize hydrocarbons extracted from decaying leaf litter, may suggest that microorganisms, or their products, are an important food source for earthworms. Worms may ingest soil and organic matter inhabited by large populations of microorganisms, crush the soft-bodied organisms in the gizzard and then extract nutrients in the gut. The remaining materials, shredded litter, cell wall fragments etc., are a favourable environment for rapid increases in microorganism biomass in earthworm faeces. LITERATURE REVIEW / 14
3. Impact of earthworms on the soil system
a. Effects of earthworms on soil structure and fertility
Earthworms have been found to have a major impact on the soil system. Lee (1985), Springett and Syers (1984), Hayes
(1983), Edwards (1981), Kirkham (1981), Edwards and Lofty
(1977) and Satchell (1967) summarized the effects earthworms have on soil structure. Soil with worm casts contained more water-stable aggregates than non-cast soils and had higher porosity. Crops grown on soil in which earthworms were active, showed higher yields through better root penetration and nutrient availability. Decomposition of organic matter may be enhanced through mixing and shredding by earthworms and the proliferation of fungi and bacteria (Shaw and
Pawluk, 1986)
b. Effects of earthworms on infiltrability
The infiltrabi1ity of water into the soil has been related to earthworm activity. Carter et al. (1982) reported that infiltration rates in drained and undrained fields in the
Fraser Valley, British Columbia, positively correlated with earthworm abundance. Ehlers (1975) reported on the
infiltration of water in tilled and untilled plots. He concluded that earthworm channels contribute to water drainage only when they reach the surface and that water LITERATURE REVIEW / 15
infiltration will take place only at high rain intensities.
Baker (1981) concluded from his literature review that earthworms increased the infiltration rate of water into the
soil. His research also showed that when earthworms were
removed from a turf grass putt and pitch, through application of pesticides, the burrows rapidly closed and
the infiltration rate decreased.
c. The mixing of organic matter into the profile
Mixing of organic matter into the soil profile by
earthworms, and the changes in the profile were studied to
describe the effects worms have on the soil profile. Dietz
and Bottner (1981) placed 1UC labelled litter on the surface
of a grassland soil and used autoradiography to follow the movement of the 1"C into the profile. Most of the
decomposition products were transported by drainage, while a
small portion was mixed into the soil by earthworms. Stout
(1983) and Stout and Goh (1980) showed that "bomb carbon"
(1WC enrichment of the biosphere from nuclear bombs) was not
mixed in the profile by surface dwelling worms in a forested
system in England, but was mixed into the profile by
sub-surface dwelling worms. Sub-surface or endogeic species
do not mix surface litter into the profile (Shaw and Pawluk,
1986), however, endogeics may mix "bomb carbon" into the
1 profile because "C02 is taken up by shoots and the LITERATURE REVIEW / 16 radioactive material is translocated to the roots. Partly decomposed roots are ingested by endogeics and the "bomb carbon" is cycled by these worms. The "bomb carbon" was also mixed into the profile by introduced earthworms in a grassland in New Zealand. Radiolabelled Cs was followed in a field trial in Oakridge, Tennessee by Crossley et al.
(1971). Earthworms (Oclolasion I act eum) mixed the label into the mineral soil. L. terrestris, introduced in coal spoils, removed large quantities of litter from the surface
(Vimmerstedt and Finney, 1970).
Earthworms that invaded a New Brunswick mixed forest,
Al I ol obophor a tuberculata, Dendrobaena oclaedra, L. festivus and L. terrestris, dramatically changed the soil profile
from a typical Podzol to a profile with an apparent Ah horizon. This transformation took place in approximately 4 years (Langmaid, 1964). Improved soil structure and a decrease in thatch were observed after earthworms, A.
caliginosa and L. terrestris, were introduced in newly
reclaimed polders in The Netherlands (Hoogerkamp et al.,
1983). When earthworms were removed from an orchard soil in
The Netherlands through over-use of copper-containing pesticides, the soil structure rapidly deteriorated and a thatch layer developed on top of the mineral soil (Van Rhee,
1963). LITERATURE REVIEW / 17
Thus, some earthworm species clearly play a role in the draining characteristics of soils and in the mixing of organic matter into the soil profile. Worms can drastically change the profile; this change may not be permanent once earthworms are removed from the soil system.
d. Surface cast production
Researchers first studied worm-cast production by collecting only a few samples per field. These samples were scraped from the soil surface and would not represent the cast production in a larger field (Evans and Guild, 1947). Evans and Guild (1947) collected casts on a much larger scale.
They sampled from 1 m diameter plots and estimated an annual production of 31.4 t.ha"1. Only two species, AlI ol obophora
I onga and A. nocturna, both surface casting worms, were noted to contribute to the surface cast (Evans, 1948).
Recently, wormcasts were collected from several plots per field to quantify the cast production of tropical species.
Watanabe and Ruaysoongnern (1984) collected surface casts of the genus Pheretima in Thailand. Casting activity took place
in the rainy season, June to November, and the production ranged between 132.6 and 224.9 t.ha~1.y~1. The cast production of Pheretima alexandri in India was described by
Reddy (1982). This species produced between 23.4 and 140.9 LITERATURE REVIEW / 18 t.ha_1.y_1 in a humid mixed woodland. Data on surface-cast production of different earthworm communities were compiled by Lee (1985), Watanabe and Ruaysoongnern (1984), Reddy
(1983), Edwards and Lofty (1977), Evans (1948) and Evans and
Guild (1947). Annual surface cast production varied between
4.5 and 90.2 t.ha"1 in temperate regions with lumbricids, and between 50.4 and 2600 t.ha"1 in tropical regions. No data were found in the literature specifying total cast production (surface plus sub-surface cast) in the field.
e. Parameters affecting the cast production of earthworms
Parameters affecting cast production of earthworms were studied for several species. Lavelle (1975) related food consumption and growth of Millsonia anomala, a tropical earthworm, to soil water potential. Maximum worm activity was occurred at pF 2.0 - 2.5 (1.0 - 3.1 m of water); worms became inactive when the pF rose to between 3 and 4.2
(10 and 160 m of water). Bouche (1983), specified the pF ranges for earthworm species: the pF limits for anecics were
2.06 - 3.08 (1.1 - 12 m of water), for epigeics, pF
2.31 - 3.33 (2 - 21 m of water), while for endogeics no limits were established.
The cast production was influenced by soil temperature: temperatures up to 30 °C increased cast production of M. LITERATURE REVIEW / 19 anomal a (Lavelle, 1975), and temperatures in the 5-10 °C range increased feeding and burrowing activity of
AlI ol obophora rosea (Bolton and Phillipson, 1976).
Immature worms of the species M. anomala showed a relative intake of soil 3 times higher than that of adults (30 °C)
(Lavelle, 1975). This phemomenon was also reported by Bolton and Phillipson (1976) for A. rosea, although the difference between very young worms and adults was much smaller.
Differences in energy budget (food intake) between small immature, large immature and adult worms, illustrate the changing metabolic demands of individuals through their life cycle (Lee, 1985).
Food quality influenced the total cast production as was described by Martin (1982). He mixed grass meal with soil and found that the egestion rate of L. rubellus decreased when more grass meal was added to the mixture. Lavelle et al. (1983) added hydrocarbons, extracted from leaf litter, to soil on which M. anomala fed. U. anomal a showed a decreased cast production when increased amounts of hydrocarbons were added to the soil, while the worms continued to grow. Hydrocarbons may have increased the food value of the offered soil, because they include nutrients produced by or extracted from microorganisms in the litter LITERATURE REVIEW / 20 from which the hydrocarbons were extracted.
Cast production of L. rubellus and A. caliginosa depended on the calcium concentration of the soil. Calcium added to a field in New Zealand, increased the surface cast production of those species (Springett and Syers, 1984).
In summary, total cast production of earthworms may be positively affected by soil moisture, soil temperature and calcium concentration, while increased food quality decreased the amount of casts produced. The age of the worm is a significant factor in the cast production: young immature earthworms have a higher egestion rate than clitellated adults. LITERATURE REVIEW / 21
B. LUMBRICUS RUBELLUS HOFFMEISTER, 1843.
1. Distribution
The earthworm Lumbricus rubellus Hoffmeister, 1843,
(Annelida, Lumbricidae), inhabits humus rich moist soils
such as in pastures and riverbanks, under stones, boards or decaying leaves (Reynolds et al., 1974). drained agricultural fields (Carter et al., 1982; Carter,
unpublished). It is perhaps the most widespread species in
the world. It has been reported in Europe, North America,
Australia and New Zealand (Robotti, 1984). Reynolds et al.
(1974) described it as one of the most widely distributed
and abundant species in Eastern North America: the worm is
recorded in 25 states of the US and 6 Canadian provinces. It
is a common species in the Vancouver area in drained
agricultural fields (Carter et al., 1982; Carter,
unpublished). However, no records were found on L. rubellus
in the prairie states and provinces.
The dispersal of this species, and of earthworms in general,
was described by Lee (1985), Bouche (1983), Schwert (1980)
and Gates (1976). Passive migration of earthworms may take
place by water, land slides and animals including humans.
Most North American species were introduced from Europe by
immigrants bringing farm animals and plant stock. Further LITERATURE REVIEW / 22 distribution of worms in Canada took place through plant stock and livestock shipments, spreading of manure and by fishermen discarding surplus bait.
L. rubellus is usually found in the upper 8 cm of the soil
(Edwards and Lofty, 1977) and according to Byzova (1965), it moves down during dry surface conditions but is found in the litter layer under very wet conditions. Persson and Lohm
(1977) reported that L. rubellus was found in the 15-30 cm depth of a grassland soil in Sweden. The species is capable of surviving a wide range of conditions (Curry and Cotton,
1983; Eijsackers, 1983). Conditions under which L. rubellus may be found, are listed in Table 1.
Reynolds (1976) described the species as a pioneer species, and Lee (1985) noted that L. rubellus appeared early in the development of a pasture system, but later was found as a minor component. Bengston et al. (1979) suggested that the survival of A. caliginosa was superior to that of
L. rubellus in introductions using litterbags in an Iceland hayfield.
In Europe, L. rubellus is not a dominant species (Edwards and Lofty, 1977; Van Rhee, 1963); however, Eijsackers (1983) reported it to be present in great abundance in abandoned LITERATURE REVIEW / 23
Table 1. The conditions restricting the distribution of L. rubellus
Parameter Value Reference
pH 2.5-9.0 Lofs-Holmin (1983)
temp, optimum 15 - 18° C Edwards and Lofty
(1977)
soil moisture moist soils Reynolds (1974)
texture clay - gravely sand Edwards and Lofty
(1977)
light loam Ma (1983)
altitude lowland to alpine Zajonc (1982)
fields in The Netherlands. L. rubellus is commonly found in association with AlI ol obophora rosea, A. longa, A.
caliginosa, A. chlorotica, Lumbricus castaneus, and L.
terrestris (Zajonc, 1982; Edwards and Lofty, 1977).
In Coastal British Columbia, L. rubellus is a dominant species in drained silty clay loam soils, with maximum densities ranging from 13.1 to 25.0 g.m"2 (dwt) (Carter, unpublished; Carter and Bandoni, unpublished). LITERATURE REVIEW / 24
2. Reproduction
L. rubellus produces large numbers of cocoons (79 - 100 per worm per year). The cocoons incubate 10 weeks and the worms grow to maturity in 40 weeks (Evans and Guild, 1948; Edwards and Lofty, 1977). Each cocoon hatches one, sometimes two, hatchlings (Evans and Guild, 1948). Cocoon production depends on soil temperature, soil moisture, food availability and quality (Evans and Guild, 1948), and soil
texture (Ma, 1983). Ma (1983) reported that the worm showed a higher activity and cocoon production in a sandy soil, compared to a silt loam.
3. Food sources and eating habits
Food sources of L. rubellus include manure, litter or
organic matter (Edwards and Lofty, 1977), and relatively
undecomposed plant remains (Piearce, 1972). Piearce (1978)
found that the gut of L. rubellus contained an abundance of
organic matter, (mostly fibres and grass leaves) and a minor
algal component. Selective feeding by L. rubellus on algae
was also observed by Nekrasova et al. (1976). Baylis et al.
(1986) reported that L. rubellus contained 32P, added to the
leaves of clover plants and transported to the roots. LITERATURE REVIEW / 25
4. Respiration
Byzova (1965) reported an oxygen consumption rate for
L. rubellus of 89 mm3.g_1.h_1. The worm had a rate that was similar to that of midstrata and deep soil dwellers (Byzova,
1965). The specific haemoglobin content of the blood was
14.4 mg.g"1 (dwt), the lowest of the four species
investigated (Byzova, 1973).
5. Egestion and soil turn-over
Not much information is available regarding ingestion and turn-over of soil and organic matter by L. rubellus.
Martin (1982) found a maximum egestion rate of 3.01 g.g-1.day1 (live weight) for soil mixed with 4.4 g.kg"1 grass meal. The figure for soil only was 1.92 g.g-1.day1
(wet weight). A removal of 0.15 g.g-1.day1 (dwt) from the
surface was reported for hazel leaves and between 0.32 and
0.40 g.g-1.day1 (dwt) for manure (Edwards and Lofty, 1977).
Carter et al. (1983) reported an egestion rate for soil of
1 1 0.90 g.g" .day , using a chromium oxide (Cr203 ) technique.
Sharpley and Syers (1977), and Syers et al. (1979) reported maximum surface cast production by L. rubellus in grassland
soils in the spring and fall, which they could relate to
soil moisture and temperature. Heungens (1969) reported a decrease in litter depth through the shredding of pine
litter by a community of Lumbricids, mainly Dendrobaena spp. LITERATURE REVIEW / 26 but including L. rubellus, L. castaneus, Eisenia eiseni and
A. cI or ol i ca .
When lime was applied to a field, L. rubellus produced significantly more surface cast than without lime. In the laboratory, the worm tended to mix lime and phosphate rock horizontally in the profile, while A. caliginosa mixed vertically (Springett, 1983).
6. Ecological classification and strategies
Bouche (1977) classified L. rubellus as an epigeic species
(small worms, high reproduction, living in the litter layer), although the worm has also characteristics of the anecics (burrowing). In Julin's system (Reynolds, 1976), the worm was described as a hemerobiont, closely tied to human populations. Satchell (1980) described the survival strategy of L. rubellus as that of an r-strategist (high reproduction, fast recovery), although the worm was reported to have some characteristics of the K-strategist, for example its moving into the soil profile under adverse conditions.
The species could adapt itself to many conditions and has been regarded as a pioneer species. The worm ingests soil and relatively undecomposed plant material and may select LITERATURE REVIEW / 27 microorganisms as food. Limited information is available on soil turn-over, and no information was found on the distribution of casts in the soil profile. The fact that the species did not exactly fit in either the survival or the strategy classification might explain its adaptability and widespread distribution. III. THE EFFECTS OF SOIL MOISTURE AND SOIL TEMPERATURE ON
THE EGESTION AND INGESTION RATES OF LUMBRICUS RUBELLUS
HOFFMEISTER
A. MATERIALS AND METHODS
1. Introduction
The redistribution of organic matter in the soil by
L. rubellus may be influenced by the soil temperature and soil moisture content. The effects of temperature and moisture on the cast production of the earthworm L. rubellus was quantified, using a litterbag technique. In this study it was assumed that the temperature and moisture regimen of the soil do not affect the earthworm activity, measured as the amount of soil and organic matter ingested or egested.
The effects of drought stress on the earthworm were discussed using the results of the litterbag experiment.
2. Site description
The study site was located on Westham Island (122°.30' W,
49°.36' N) , 55 kilometres south of Vancouver, B.C., situated
in the delta of the Fraser River. The soils were of fluvial origin and were classified by Luttmerding (1981) as silty clay loam-textured Orthic Gleysol (typic haplaquept in the
US classification) of the Crescent Series. To improve
28 MOISTURE AND TEMPERATURE / 29 agricultural production, the original, poorly-drained soil had been drained with perforated plastic drains, spaced 20 m apart and situated at a depth of 1.2 m. The drains emptied into a ditch that was pumped year-round.
During 1983, field data were collected from the experimental plot. The plot (35 by 35 m) was in the clover phase of a barley-clover-potato rotation. During the second year of this study (1984) the part of the field that was used for the experiment was kept under clover, while the remainder of the field was under potatoes.
3. Field data collection
During the two years in which the experiments were conducted, soil temperature and gravimetric soil moisture content were measured. The soil temperature at 5, 10 and 15 cm depth was continuously recorded using a thermograph, and twice monthly, six soil samples were taken in a pre-designated sub-plot to determine the soil water content.
These samples were taken from the 0-5 cm layer and the 5-10 cm layer. MOISTURE AND TEMPERATURE / 30
4. Earthworms used in the experiments
The earthworms used in the experiments, were Lumbricus rubellus Hoffmeister, 1843 (Annelida, Lumbricidae), collected from the clover field on Westham Island by handsorting. Only clitellated adults were collected prior to each experimental run.
5. Sample collection
Soil was collected from the plough layer, after the top 3 cm was removed and discarded because this layer contained large amounts of earthworm casts and had a root mat. Clover hay was collected in the spring after it had been in the field during the winter months. Soil and clover hay were stored in the freezer and were left to thaw several days prior to each trial. The organic material was washed in tap water to remove old faecal material and soil, and cut into 1 cm pieces. The soil was broken into aggregates of about 1 cm in diameter.
Soil collected on Westham Island was also used to create a stable environment with a known moisture content. This soil was broken into aggregates < 0.5 cm and brought to the desired water content by watering with a plant sprayer and mixing by hand. MOISTURE AND TEMPERATURE / 31
6. Litterbag technique
Ingestion rates and egestion rates of L. rubellus were estimated using a litterbag technique (Carter, personal communication). Often, litterbags are used for decomposition studies. The exclusion of soil organisms and the easy recovery of plant materials is the main purpose for the use of the bags (McBrayer and Cromack, 1980; Uvarov, 1982). The mesh size is related to the size of organism to be excluded.
Bags of various size mesh have also been used to contain soil and organisms in experiments to measure growth and reproduction (Satchell, 1971) and survival (Bengston et al.,
1979) of earthworms and of ingestion and egestion studies of millipedes (Carter, pers. communication).
In using litterbags to study the food uptake and egestion rates of contained organisms, the mesh size should be sufficiently small to contain the animals and their casts, but not too small to impede gas and water exchange. Uvarov
(1982) reported difficulties with water exchange in litterbags placed in the field, especially for those with a mesh size of < 0.01 mm.
Litterbags were made from fine mesh polyester material
(no-see-um netting, 0.3 mm mesh size), measured 10 by 10 cm, and were assembled by stapling a strip of plastic on the MOISTURE AND TEMPERATURE / 32 folded hems. The bags were closed by stapling the twice-folded hems. The 0.3-mm mesh size was assumed to be large enough not to impede gas and water exchange. Partially dried material was used for the lower water contents and water was added to the content of the bag for the higher moisture levels, to prevent possible effects of a small mesh size.
To indicate the moisture status of the soil, the soil water tension (metres of water) or the soil water potential
(metres of water or Joules.kg"1) was used. These units indicate the energy state of the water in the soil (Hillel,
1980). Soils with similar potentials could then be compared as to the effects on earthworms or plants. The relationship between soil moisture and the soil water tension is described as the retention curve (Hillel, 1980). When the soil moisture content is used, a complete description of the soil, including a retention curve, should be provided to relate the moisture content to soil water potentials. The retention curve for the Crescent silty clay loam is included in Appendix 2-E.
Soil water potential has been used for indicating the moisture status of the soil in several earthworm studies.
Evans and Guild (1948) related the cocoon production of MOISTURE AND TEMPERATURE / 33 earthworms to pF values, the log transformation of the soil water tension in centimetres of water. Lavelle (1975) related the ingestion of soil by tropical earthworms to the pF values and Reynolds and Jordan (1975) advocated the use of soil water tensions in habitat descriptions. Bouche
(pers. communication) advocated the use of soil water potential ("...II est essentiel que vos resultats soient
exprimes en pF ... car le % H20 ne veut rien dire !...").
Earthworms were starved for 48 hours at incubation temperatures (5, 10, 15 and 20 °C), then put into the litterbags containing a pre-weighed amount of food, consisting of a mixture of soil and clover hay. The bags were buried in large plastic washbasins, filled with moistened soil. The basins were covered in plastic to prevent evaporation and were kept in the incubator for seven days. The loose packing of soil aggregates in the basins and the large volume of air between the plastic and the soil, prevented anaerobic conditions. In preliminary tests it was found that the soil showed virtually no difference in water content before and after a feeding trial; therefore the moisture content of the filler soil was measured at the end of the experiments. The following moisture levels were used in the experiments : 0.33, 0.30, 0.27 and 0.24 kg.kg-1 (-5,
-9, -17 and -25 m of water respectively). Higher soil MOISTURE AND TEMPERATURE / 34 moisture contents were not used because of smearing of soil and faecal material by the worms. Thirty worms, each in a
separate litterbag, were incubated in each moisture-temperature combination.
No significant difference in egestion rate (g.g"1.day"1) between 7, 10 and 14 days incubations was found in preliminary tests. Therefore subsequent experiments were run
for 7 days (See Appendix 3-A). Fresh faeces may contain a
high level of ammonia, which might be toxic to earthworms as described by Neuhauser et al. (1980 a) for Eisenia foetida
in experiments lasting for one month. Based on the short
duration of the present experiments it can be assumed that
no cast material was consumed and no toxic build-up of
ammonia took place.
After incubation, the worms were removed from the litter
bags. With a glass rod the anterior end of the worm was massaged until a small amount of cast was produced (Bolton
and Phillipson, 1976). The cast material was then
immediately transferred onto a pre-weighed aluminum dish and
weighed on a micro balance. After being oven-dried (4 days,
65 °C), the cast was weighed again and the water content was
calculated. The worms were then starved for 48 hours to
remove their gut content, and freeze-dried to determine MOISTURE AND TEMPERATURE / 35 their dry weights. Faecal pellets were sorted out and the components of the leftover food were separated, oven-dried
(4 days, 65 °C) and weighed.
7. Water content of the worm
Soil of the Crescent series was partially dried and crushed sufficiently to pass a 2 mm seive and was then equilibrated in a porous plate extractor to reach predetermined soil water potentials between -3 and -60 m of water. After equilibration, the soil was transferred into plastic containers and 5 earthworms were added to each container.
Sub-samples were taken, dried and weighed to construct a retention curve. The experiments were done in duplicate for both adult and immature adult earthworms. The latter were well developed non-clitellated specimens.
After incubating seven days at 19 CC in the closed containers, the worms were weighed and then placed in Petri dishes on moist filter paper to have their gut emptied. The faeces were collected, air-dried and weighed. The worms were immediately killed by freezing, dehydrated in the freezer and weighed. The water content of the"worms was calculated assuming that the gut content contained 53 % water (dwt), the liquid limit of the Crescent soil (De Vries, personal communication). MOISTURE AND TEMPERATURE / 36
8. Chemical analysis
Total carbon of soil and cast materials was determined by
dry oxidation, using a Leco carbon analyser.
9. Calculations and Statistics
The experiment was designed as a 4X4 factorial, with equal
spacing beween temperature and between moisture levels.
Normality was tested using skewness and kurtosis of the
standardized population, the homogenity of variances was
tested and appropriate logarithmic transformations were
applied. Functions were fitted for linearity, quadratic or
cubic relations and the probabilities of the contrasts were
calculated. The equality of the means was tested with a
series of student t-tests (egestion experiment) or a series
of Mann-Whitney U-tests (water content of the worms).
B. RESULTS AND DISCUSSION
1. Litterbag technique
Faecal material was easily separated from the left-over food
because of the distinct shape and structure of the pellets.
Their rounded shapes were different from the angular soil
aggregates and their colour was darker and greener than the
bulk soil. MOISTURE AND TEMPERATURE / 37
2. Calculations and statistics
a. The grouping of the moisture and temperature levels
The experiments involving egestion rates, were conducted at several moisture levels, but incubated at constant temperatures. The drawback of this approach was that the moisture regimens were not exactly the same in each temperature trial. However, when grouped, the midpoints of the ranges (moisture content, kg.kg"1) were equally spaced and therefore a factorial approach in the statistical analysis was used.
b. Calculation of the ingestion rates
The calculation of the ingestion rate was difficult, because individual input and output values had to be used while the correction for the water content was based on bulk measurements. The food material was not dried before it was put in the litterbag, because a change in physical, chemical and especially microbiological characteristics, would have resulted from drying.
c. Statistical analysis
Equal numbers of data points per stratum are required for
ANOVA tests. As the number of data points varied between 24 and 30, due to worm mortality and escapes, the number of MOISTURE AND TEMPERATURE / 38 data points was reduced to 24 for each stratum. There are several methods to reduce the number of data points. The method used was that of 'reasoning - out' cases. Outliers were examined and if there was reason to believe that the value could be explained as not a normal one, these points were deleted from the data set. Care was taken that both high and low outliers received a similar treatment.
Preliminary tests showed that about 50 % of the variability was caused by only 10 % of the cases in a certain set. The equalized data sets were normally distributed. They were tested for normality by describing the skewness and kurtosis of the standardized distributions. Also a Lilliefors test did not reject the hypothesis that the egestion rate was normally distributed (p > 0.10). To homogenize the variances, the data was exponentially transformed. Powers of transformation were calculated assuming V(ju) = hu . The calculated powers were: 0.07489 for the egestion rate (E),
0.0959 for the ingestion rate of organic matter (IOM),
0.0951 for the ingestion rate of soil (ISOL) and a ln transformation for the total ingestion rate (ITOT = IOM +
ISOL). After transforming the data, the variances were still not significantly homogenous, but the large number of replications in each stratum (24) made the use of parametric statistics possible (Siegel, 1980). As a precaution, the separation of means was tested with an F-test and a MOISTURE AND TEMPERATURE / 39
(non-parametric) Kruskal-Wallis K-sample test. The two tests gave similar significant results (p < 0.01).
d. Curve fitting
The factors Temperature and Moisture as well as the T*M
interaction were significant for all variables (Table 2).
Matching curves through testing orthogonal polynomials
(curve fitting) yielded many significant interactions and it was not possible to draw any conclusions regarding type of curve, inflextion point or threshold values. Therefore, the
equality of means was tested with a series of t-tests. The data points in Figure 2 were connected by hand.
3. Egestion rates of soil and organic matter
Both temperature and moisture clearly influenced the egestion rate of L. rubellus. In wet soil a significant difference was found between the egestion rates at various
temperatures (Table 3). When the soil wetness decreased from
0.33 to 0.30 kg.kg'M -5 to -10 m of water), the E did not change significantly. At a lower moisture level, (0.27
kg.kg"1, - 17 m of water), the E increased significantly for
all temperature trials except the highest temperature (20
°C), where it decreased significantly. In this case, the
egestion rate for dry soil (0.24 kg.kg"1, -25 m of water)
was significantly lower than for medium dry soils. The MOISTURE AND TEMPERATURE / 40
Figure 2. The egestion rate (g.g"1.day"1) of L. rubellus related to the soil temperature and the soil moisture. Each point represents 24 worms. MOISTURE AND TEMPERATURE / 41
Table 2. F-values for interactions and contrasts describing Egestion and Ingestion rates of L. rubellus, incubated at different moisture contents and set temperatures. (** p<0.01, * p<0.05, n = 24)
Egestion Ingestion (OM) Ingestion (SOIL)
TEMP 63 . 7** 5 . 76** 53.6** MOIST 113.8** 8.6 6** 9 8.7** T*M 39.0** 3.91** 34. 5**
TLin 136.2** 6.84** 99.3** TQuad 514 . 9 * * 6.71** 61.3** TDev 0.05 3.37 0.052
MLin 169.4** 0.21 163.44* MQuad 127.2** 12.4** 96.9** MDe v 44.9** 13.3** 35.9**
TLin-MLin 99. 5** 0.04 88.5** TLin-MQuad 16 5.6** 0.46 151.3** TLin*MDev 18.5** 20. 3** 4.2 3* TQuad-MLin 5.8 8* 0. 54 4.70* TQuad-MQuad 54.6** 0.28 52.3** TQuad*MDev 0 .26 0.37 0.04 TDev-MLin 4.82* 7.06* 5. 82* TDev-MQuad 0.61 0.13 0.77 TDev-MDev 5 .09* 6 . 00* 2 .46 Table 3. Egestion rates for L. rube HUH, incubated at different temperatures and moisture regimens. Probability of data points being different (t-test, * = p < 0.0S, ••••• = p < 0.01, n=2M).
A. Temperature gradient compared.
Moisture content: •1 0.33 kg.kg 0. 30 0. 27 0. 2U
Temp. Temp Temp Temp 5° C. 5° C. 5° 5° C 10 10 10 10 lb ;'; 15 1; 15 5*; & 15
20 &;» 20 20 :V 20 :'; sV o Temp 5° 10 15 5 10 15 5 10 15 5 10 15 I—I tn -9 G
B. Moisture gradient compared > Z Temperature: D 5° C. 10 15 20 -3 M 3 0.33 0.33 0.33 0.33 0.30 0 . 30 0. 30 0. 30 M 0.27 0 . 27 0.27 0. 27 > -3 0. 2<4 0. 2M 0. ?t 0. 21 C n Moisture 0.33 0. 30 0.27 0. 33 0. 30 0.27 0.33 0.30 0.27 0.33 0.30 0.27 MOISTURE AND TEMPERATURE / 43 general trend was that when the soil moisture content decreased, the egestion rate increased and then dramatically decreased. In wet soils the temperature effect was noticable. In medium wet soils(-lO to -15 m of water), the moisture effect obscured the temperature effect, while in dry soils (< -20 m of water), the moisture effect was important. The effects of the dry soil was more visible at 5
°C and 20 °C, probably because these temperatures are near the limits of the temperature range of the worm.
4. Egestion rate of carbon
The egestion rate of carbon was calculated from the carbon content of the faecal material and the egestion rate. A significant positive temperature effect (Kruskal-Wallis
K-sample, p < 0.01) was found (Table 4). The earthworms processed less carbon at 5 °C than at all other temperatures. At 5 and 20 °C, the dryest soil showed a significantly lower egestion rate of carbon (Mann-Whitney
U-test, p < 0.05, p < 0.01), while at 15 °C, the egestion rate of carbon in wet soils was significantly lower than that of the 0.27 kg.kg"1 moisture level (p < 0.01). No significant differences were found between the treatments at
10 °C. A threshold limit may affect the activity of the earthworm. The egestion of carbon seemed to reach a maximum at approximately 0.27 kg.kg"1 moisture ( - 17 m of water) MOISTURE AND TEMPERATURE / 44
Table 4. The comparison of the total egestion rate, E (total) (g.g~1.day~1, SD) with the egestion rate for carbon, E (carbon) (mg.~1.day~1, SD) for four temperatures, T ( °C) and four moisture contents in each set of temperatures (0.33, 0.30, 0.27 and 0.24 kg.kg"1 respectively)
T E (total) (SD, n=24) E (carbon) (SD) n
5 0.31 (0.061) 17.8 ( 6.40) 10
0.31 (0.078) 18.1 ( 5.28) 12
0.41 (0.195) 25.9 ( 5.95) 9
0.15 (0.063) 12.7 ( 4.51) 8
10 0.46 (0.117) 37. 1 (12.31) 14
0.44 (0.080) 35.6 (12.24) 12
0.53 (0.179) 39.8 ( 7.05) 8
0.40 (0.106) 40.8 ( 7.66) 1 1
1 5 0.51 (0.089) 34.3 (12.51) 10
0.48 (0.124) 34.0 ( 7.92) 14
0.73 (0.296) 51.1 (16.03) 14
0.49 (0.133) 40.8 ( 8.71) 9
20 0.91 (0.253) 47.7 (12.98) 1 1
0.97 (0.416) 50. 1 ( 8.30) 1 1
0.67 (0.388) 47.9 (10.85) 9
0.31 (0.769) 19.4 ( 8.76) 1 3 MOISTURE AND TEMPERATURE / 45 before it decreased rapidly as the moisture content decreased further. Mitchell (1983) reported on a similar threshold for the egestion rate of E. foetida, feeding on sewage sludge.
The egestion rate of carbon is a more "stable" parameter than the total egestion rate, even when a lower number of data points per stratum due to incomplete data sets, were considered (n=24 vs n=9-14).
5. Q10 values of the activity of earthworms
The egestion rate of earthworms may be seen as an index of earthworm activity because it represents their nutritional needs, and indirectly reflects the respiration. Phillipson
and Bolton (1976) discussed the Q10 values (the change in respiration rate over a 10 °C interval) for AlI ol obophora rosea and concluded that it was essential to know the temperatures covering the interval, before any statements could be made. Howard (1971) showed a decrease in
theoretical Q10 values with higher temperature intervals in case of a linear response to increasing temperatures.
The Q10 for L. rubellus, based on the egestion rates, varied with the temperature range and with the moisture content of the soil (Table 5). Because the egestion rate of worms MOISTURE AND TEMPERATURE / 46
Table 5. The Q10 of L. rubellus, calculated from the egestion rate, for different moisture and temperature ranges. Worms were acclimatized at the incubation temperature. The incubation lasted for 7 days.
Q10 for the total egestion rate
Temp. Moisture (kg.kg~1)
0.33 0.30 0.27 0.24
5 - 15° 1.66 1.55 1.78 3.27
10 - 20° 1.98 2.20 1.25 0.77
Q10 for the egestion rate of carbon
5-15° 1.92 1.88 1.97 3.21
10 - 20° 1.28 1.40 1.20 0.47
incubated at 10 and 15 °C is less influenced by drought
stress than at 5 and 20 °C, the trend in Q10 differed for
each temperature range. In wet soils, an increase in Q10 was observed with increasing temperatures, contrary to what
Howard (1971) expected. Large changes in Q10 became apparent, especially in dry soil. MOISTURE AND TEMPERATURE / 47
The Q10 for the egestion rate of carbon showed a similar trend with moisture content, while the temperature effect
(5-15 vs 10-20 °C) was reversed. The Q10 followed the theoretical decrease with a higher temperature interval, as described by Howard (1971). The values close to 2.0, for the lower temperature interval, are similar to those reported as a general value for earthworms by Phillipson and Bolton
(1976).
6. Faecal organic matter
The amoiint of organic matter, measured in earthworm faeces indicates the feeding pattern of worms. Faeces may show a higher organic matter content than the soil earthworms feed on, indicating that worms selectively ingest organic matter.
Table 6 shows both the measured organic matter content of the faeces and the ingested amount, calculated from organic matter recovered from the litterbags and the amount originally present. Although there is inconsistency between measured and calculated values because of the difficulties in the recovery of organic matter from the bags, an increase in organic matter content with increasing soil dryness is visible in both the measured and calculated values.
L. rubellus ingested relatively more organic matter when incubated in soil with a low soil water content. This trend is not apparent at 10 and 15 °C, because these temperatures MOISTURE AND TEMPERATURE / 48
Table 6. The percentage of organic matter ingested by L. rubellus at indicated soil moisture levels and temperatures, and calculated from IOM and ITOT and measured in the faeces.
% Organic Mattert
Temp °C Moisture content
0.33 0.30 0.27 0.24
Calc. Meas. Calc. Meas. Calc. Meas. Calc. Meas.
5 14.5 9.7 16.9 10.4 14.8 9.4 31.5 14.8
10 14.6 13.9 19.8 14.1 11.7 14.3 7.2 18.9
15 5.7 12.7 7.2 11.4 15.3 12.1 13.5 13.9
20 10.5 9.2 10.8 11.9 19.2 14.1 36.5 21.3 t A conversion factor of 1.724 was used to calculate % OM from % C measured in the faeces.
are close to the optimum temperature for the species. The earthworms are less affected by drought stress at . these temperatures. Also the egestion rates show this phenomenon.
The worms might ingest (and thus egest) more organic matter because this material provided moisture to the worms, for it MOISTURE AND TEMPERATURE / 49 contained more water than mineral soil. The liberation of water through the assimilation of organic matter is less likely, because worms assimilate only small quantities of organic matter and they are less active in dry soils.
The carbon content of the faeces was above the carbon content of the soil, indicating that a mix of organic matter and soil was taken as food. Lee (1985) compiled data on the carbon content in earthworm casts. For L. rubellus he reported 4.3 % carbon (7.4 % OM) for casts from pastures and
1.3 % carbon (2.2 % OM) for casts from pot experiments. The values for pastures are close to those found in the present research for worms not under drought stress.
7. Faecal water content
It was noticed that faecal material with a high water content also contained a high amount of organic fibres. The faeces water content for each worm recovered from the litterbags, was measured at the end of the incubations. The faeces water content varied between 0.53 kg.kg"1 and 2.4 kg.kg"1, and was always above the liquid limit of the
Crescent soil, indicating that the faeces was produced as a slurry. The production of slurry-like faeces was observed both in the laboratory and the field. In the field, water was rapidly absorbed into the soil on which the faeces was MOISTURE AND TEMPERATURE / 50 deposited. The slurry-like faecal material could only be observed immediately after the worms produced it.
8. Ingestion rates
The rates of ingestion of mineral soil and organic matter, both calculated from recovered materials, showed a similar trend as the egestion rate did (Figures 3 and 4, Tables 7 and 8). In wet soils a positive temperature effect was clearly visible, both for the ingestion of organic matter and of soil. The ingestion of mineral soil peaked at a medium moisture content, except at 20 °C, where it peaked at a higher soil moisture content. The ingestion rate of organic matter showed a less reliable trend, probably because of errors in the recovery of the materials from the litter bag. Organic matter particles were sorted out by hand. Some of the material was finely shredded and some of it was embedded in cast.
9. Worm size
Worms were collected from the field shortly before each experimental run. The size of the animals, all clitellated adults, varied over the season. Animals collected in the spring (5 °C. and 10 °C) were larger than those collected in the fall (Table 9). In preliminary experiments, immature
L. rubellus showed a higher egestion rate than did MOISTURE AND TEMPERATURE / 51
I 0 M
0 " IO - 20 -30
SOIL WATER POTENTIAL (M OF WATER
Figure 3. The ingestion rate of organic matter for L. rubellus Table 7. Ingestion rate for Organic Matter for I., rubellus, incubated at different temperatures
and moisture regimens. Probability of data points being different (t-test, - p <0.OS, = p <0.01, n - 2 H) .
A. Temperature gradient compared.
Moisture content:
0.33 Kg.kg"1 0. 30 0.27 0.21
Temp Temp Temp Temp 5° 5° 6. b° 5°d. 10 10 10 10 lb lb 15 15 20 20 20 20
Temp 10 15 10 15 10 15 10 15 2 O »—i in •-3 B. Moisture gradient compared. G »
Temperatures : > 10 15 20 O
Moisture levels PI 0.33 0.33 0. 33 0.33 s 0.30 0. 30 0. 30 0. 33 0.27 0.27 0.27 0.27 > 0.21 0.21 0. 21 0. 21 -3 G W 0. 27 0.33 0. 30 0. 27 0.33 0. 30 0.27 0.33 0. 30 0.27 0.33 0. 20 a
(SI to MOISTURE AND TEMPERATURE / 53
<
10
20" ce
15 2 05
ISOL
0 -10 -20 -30
SUIL WATER POTENTIAL (M OF WATER)
Figure 4. The ingestion rate of soil for L. rubellus Table 8. Ingestion rate of soil for L. rubellus, incubated at different temperatures and moisture regimens.
Probability of data points beiTig different (t-test, * - p o . 0 S , = p < 0. 01, n=24).
A. Temperature gradient compared.
Moisture content:
0.33 kg.kg"1 0. 30 0.27 0. 21
Temp Temp Temp Temp S' 5' 5' C. 5C 10 10 10 10 IS 15 15 15 20 20 20 20 HZ]
5? 10 IS S 10 15 S 10 IS S 10 IS 2 O B. Moisture gradient compared. to -3 Temperature: 5° C. 10 IS 20 G W Moisture content > 0.33 0.33 0.33 0.33 a 0.30 0.30 0. 30 0. 30 PI 0.27 AA A A 0.27 0.27 A A A 0.27 ,' A A A A 3: 0.24 AA A A AA 0. 21 0.21 A A 0. 21 A A A • A A TJ ft A PJ » 0.33 > 0.30 0.27 0.33 0.30 0.27 0. 33 0.30 0. 27 0. 33 0. 30 0.27 -3 G » PI MOISTURE AND TEMPERATURE / 55
Table 9. The dry weights of the earthworms used in the experiments (n=10).
Incub. Dry weight (±SD) mg.
Temp. (°C)
5 101.64 (23.19)
1 0 106.64 (30.47)
1 5 65.80 (15.43)
20 78.10 (26.23)
clitellated adults (Appendix 3-C), but weight of the adult worms was not significantly correlated with the egestion
rate.
10. Soil temperature and soil moisture in the field
The average weekly soil temperatures, measured at 5 cm, in
the clover field on Westham Island varied between 0 °C
during a cold spell in December and 18-20 °C during the
summer months. The average yearly temperature at 5 cm depth,
calculated from the monthly values, was 10.25 °C.
The moisture content of the soil (0-5 cm) in the field on
Westham Island was a steady 0.39 kg.kg"1 (-0.3 m of water)
during the rainy season, from November to March, and reached MOISTURE AND TEMPERATURE / 56 a low of 0.23 kg.kg"1 (-30 m of water) during the summer.
During the winter months, the water content was the highest in the 0-5 cm layer, but in the summer (dry season) it was the highest in the 5-10 cm layer (Appendix 2-C).
11. Comparison of ingestion and egestion rates to literature data
The ingestion and egestion rates of L. rubellus weregenerally within the ranges of those found in the literature (see Table 10). However, inconsistencies in the reporting of temperatures and moisture contents in the literature, made it difficult to compare the actual values.
The ingestion rate for organics and hazel litter (Satchell,
1967) were similar to the IOM for clover hay, and the ingestion of cow dung is close to that of a mixture of clover leaves and soil . Martin (1982) reported egestion rates on a live weight basis for L. rubellus. When those rates were recalculated on a dry weight basis, assuming worms contained 85 % water, his egestion rates were 10 to 20 times higher than those found by other authors and those found in the present study. Even if the figures were not recalculated, they were 2 to 3 times higher.
The earthworm Allobophora chlorotica , found on Westham
Island along with L. rubellus, had an egestion rate three Table 10. Some Ingestion (I) and egestion rates (E) for temperate and tropical earthworms species food temp. CO mo 1sture I or E rate Reference (kg.kg ') (g.g-' day- 1 )
Allotobophora caliglnosa sol 1 0.26 - O. 52' P tearce ( 1972 ) A. chIorotIca so 1 1 + cI over 5, 10 0.33 1.7. 2.9' Tlmtnenga (unpublished) A. rosea adults sol 1 5-15 7.1- 9.7' Phillipson and Bolton (1976) . immatures 7.5 - 12.8' Dendrobaena piatyura leaves field field 0.09 - 0. 33' Zlcsl (1978) D. depressa 1 eaves field field 0.14 - 0. 32 ' Z1CS1 (1978) LumbrIcus rube I I us sol 1 5 0.39 0.65' present study sol 1 15 0.S2' Carter et al. (1983) sol 1 20 12.8' Martin (1982) sol 1 + grass 20 20.0' Martin ( 1982) mea 1 sol 1 + clover 5-20 range 0 1. 13 - 1 .0' present study 2 O hay n woodland 1 11 ter - - 0. 16 - O. 32' Plearce ( 1972) CO -3 clover leaves 5 0.39 0. 10' present study a hazel 11tter - - 0. 14 ' Satchell (1967) * cow dung - - 0. 46 - 0..58 ' Satchell (1967) > L. t errest r is leaves 5 - 0. 12 - O. , 36 ' Raw ( 1962) 1 a 1 eaves 9 - 0. 16 - 0..2 1 Knollenberg et al. (1985) leaves 23 - 0. 40 - 1 . 20' Satchell (1967) n 1 eaves - - 0. 15 - 0 99' Van Rhee ( 1963) 3: Mi croscolex dubfus sol 1 20 .6' Abbot and Parker (1981) RJ _ _ so 11 and mu 1 ch 10 .4' Abbot and Parker (1981) > Mi II son!a anomala adult sol 1 25 0.12 33 .0' Lavelle ( 1975) Immatures sol 1 25 0.12 150' a Octolaslum lacteum leaf litter 16 - 1 .9 ' Crossley et al. ( 1971)
Ul ) Ingestion or removal from surface, ') egestion. MOISTURE AND TEMPERATURE / 58 times higher than L. rubellus when tested in the litterbag technique (See Appendix 4). A. chlorotica, an endogeic species, consumed large amounts of soil and virtually no organic matter.
The tropical worm Millsonia anomal a, an endogeic species, had an egestion rate that was 10 to 50 times higher than that of worms from temperate regions (recalculated from
Lavelle, 1975). Mi cr os col ex dubi us , another tropical species, also showed a high egestion rate (recalculated from
Abbot and Parker, 1981). If these values are representative for all tropical earthworms, it could be said that tropical worms "work harder" than worms from temperate regions. MOISTURE AND TEMPERATURE / 59
12. Drought-survival strategies of Lumbricus rubellus
a. The water content of earthworms
The water content of adult L. rubellus varied with the soil water potential (Figure 5). No significant difference
(Kruskal-Wallis K-sample) was found between the body water content (BWC) for immatures subject to varying water potentials, but the BWC of the adults was significantly influenced by the soil water potentials (Mann-Whitney
U-test, p < 0.05, Table 11). Immatures may have different ways to hold or extract water than adults do; they have different metabolic demands (Lee, 1985), and a higher egestion rate than clitellated adults, all of which may explain the difference between the body water content of immatures and adults in this experiment.
The relation of body water to soil water potentials was described by Kuarjaseva (1982) for Eisenia nordenski ol di when she compared the weight of worms from soils with different moisture contents with the weight of a "standard worm", a worm weighed after incubation on moist filter paper for 2 days. When her data were related to BWC and soil moisture content, a similar relationship was found as is shown in Figure 5 for adult L. rubellus. The maximum BWC was at a soil moisture content of 0.50 kg.kg"1, but a relative MOISTURE AND TEMPERATURE / 60
SOIL WATER POTENTIAL (M OF WATER)
Figure 5. The body water content of L. rubellus, incubated at different soil moisture potentials (19 °C). Table 11. Values of the Mann-Whitney U-test indicating differences between body water contents of L.rubellus, incubated for 10 days at 19° C. in soil with the indicated soil water potentials (* = p < 0.05, ** = p < 0.01).
-3
-9 23.0
•p -15 14.7* 7.0** m 3 •20 17 .0* 10.0** 48.0
O •25 15 .0* 10 .0** 49.5 47.0 Ui -30 13.5* 10 .0** 49.0 45.0 48.0 O •p •HO 29 .0 20.0* 22.0* 29.5 22.0* 20.0* cn E •60 12.5* 27.0 4.0* * 3.5** 1.0** 0.0** 8 .0** 50
> meters of water --33 -9 -15 -20 z -25 -30 -40 -60 D •-3 W n per treatment 8 8 10 10 10 10 10 10 S T3 M JO > a^3 w P3
CTi MOISTURE AND TEMPERATURE / 62 minimum in BWC in very wet soils was not included. However, the BWC of the "standard worm" was 82 % of the maximum value at 0.50 kg.kg"1. Stephenson (1945) kept L. terrestris on filter paper moistened with different saline solutions. He found that the worm weights first decreased with increasing concentrations, then increased and peaked at an external medium concentration of "60 equivalent mMol NaCl" and then decreased. The concentration of "60 equivalent mMol NaCl" was calculated to be equivalent to an osmotic potential of
-28.8 metres of- water, while the minimum was found at -14 metres of water. The minima and maxima in worm weight were independent of the type of salts used. The shape of the curve presented in his paper is similar to the one presented in Figure 5 for adults.
It was assumed that L. rubellus has a coelomic fluid with an osmotic potential of about -40 metres of water, similar to that of L. terrestris (calculated from Dietz and Alvarado,
1970, and Stephenson, 1945). L. rubellus could therefore easily absorb water from moist soil. In wet soils, the steep gradient would generate an excess of water in the worm if the water was not actively excreted (Dietz and Alvarado,
1970). The excretion of excess water was also reported by
Ramsey (1949) and Wolf (1940), who showed that L. terrestris produced large amounts of urine under saturated or semi- MOISTURE AND TEMPERATURE / 63 saturated conditions.
The brain of the worm regulates the salt content of the coelomic fluid through neuro-secretory control of dermal permeability and water loss through the nephridia (Carley,
1978; Zimmermann, 1973; Kamemoto et al., 1966). This mechanism of excretion is triggered by changes in the nerve cord induced by the salt concentration of the coelomic fluid
(Laverack, 1963). These strong active processes of water removal from the body could explain the lower body water content of the adult worms in wet soils with water potentials close to -5 metres of water. When the soil water potentials were close to zero, an increasing water content may lower the osmotic potential of the coelomic fluid of the worm and the worm may reach a steady state where incoming water is in equilibrium with the water actively excreted.
This equlibrium probably is at the body water content as described by Kuarjaseva (1982) for the "standard worm."
b. Feeding behavior of the worm as related to the body water content
The feeding behavior of L. rubellus depended on the water potential of the soil, as was described previously, and the body water content was related to the soil water potential.
It is therefore suggested that the body water content MOISTURE AND TEMPERATURE / 64 influenced the feeding habits of adult worms. In soils with high water potentials, between 0 and -10 m of water (easily available water), the worms showed a significantly lower body water content and a high egestion rate. Medium potentials (-15 to -20 m of water) created a high but constant body water content but the egestion rate dropped significantly, and in soils with a low soil water potential
(< -35 m of water), the worms lost body water (Figure 6).
Organic material that was used as food had a higher moisture content than the soil in which it was incubated (Table 12).
The worms switched to a diet high in organic matter to overcome moisture stress by eating materials that contained more water. This switch was observed both at 5 and 20 °C.
The egestion figures for 10 and 15 °C suggested that under these temperatures the worms were more tolerant to moisture stress, probably because these temperatures were not near the limits of the temperature range of the species.
In dry soil, not only was the need for water to mix into the faeces increased, but also as dry soil had a more negative water potential, the absorpton of water by the worm from its environment through the skin was reduced. To stop eating can be seen as a strategy to decrease the water loss, as was the regulation of the permeability of the epithelium and MOISTURE AND TEMPERATURE / 65
Figure 6. The body water content (kg.kg"1 (—o—) , dwt) and the egestion rate (g.g" 1 .day" 1 ) (• >• ••) of adult L. rubellus at 20 °C. MOISTURE AND TEMPERATURE / 66
Table 12. The water content of soil and clover straw incubated at 20 °C
Soil moisture Clover straw
(kg.kg-1) (kg.kg"1)
0.34 3.12
0.28 2.63
0.27 1.11
0.24 0.82
0.22 0.79
decreased activity of the nephridia. Also an "escape" reaction down the soil profile, as was noticed in the field, may be part of the drought survival strategy as is the switch to more organic matter in the diet.
Bouche (1984) classified L. rubellus as an earthworm surviving drought stress in the cocoon stage. This may be the case when soil water potentials approach the permanent wilting point ( -150 m of water, pF 4.2), but with soil water potentials > -60 m of water (pF 3.8), L. rubellus might survive in cracks and deep burrows covered in cast and mucus. Laverack (1963) reported that earthworms may lose up MOISTURE AND TEMPERATURE / 67 to 60 % of their body water and recover. L. rubellus may be able to survive periods of drought by "keeping quiet."
13. Testing of assumption
The assumption that the egestion rate of L. rubellus is not influenced by moisture and temperature is rejected. The egestion rate is temperature-dependent in wet soils and negatively influenced by low soil water potentials.
Low soil water potentials may have influenced the water balance of L. rubellus and forced the worm to change its behavior (e.g. stop feeding, ingest relatively more organic matter, burrow down and create a "moist environment." IV. THE TRANSPORT OF ORGANIC MATTER INTO THE SOIL PROFILE BY
LUMBRICUS RUBELLUS
A. MATERIALS AND METHODS
1. Introduction
The transport of mineral and organic matter into the soil profile as,well as the distribution of casts in the profile was quantified by using a column experiment. In this column experiment, earthworms were fed with 14C labelled clover shoot and root litter and the cast was sorted from the columns. The recovered 1ttC activity was used to calculate the shoot to root ratio in the diet of the worm. It was assumed that L. rubellus, as an epigeic species, ingests materials only from the surface litter and produces all casts in this layer; this assumption is based on the hypothesis that L. rubellus is an epigeic species.
2. Animals used in the column experiment
The earthworm, Lumbricus rubellus was collected from a farmer's field near Abbotsford, B.C. This field had been in pasture for six years and had received annual applications of dairy cattle manure as slurry. At the time of collecting, the field was ploughed to be put into silage-corn. The soil
in this field, classified by Luttmerding (1981) as Orthic
68 TRANSPORT OF SOIL / 69
Humic Gleysol of the Buckerfield series, was of a similar texture class as the Crescent series soil used in the column experiment described below.
3. Soils used in the column experiment
Soils used for the column experiment were collected from a farmer's field on Westham Island. The field had been under potatoes the previous growing season. The soils were of fluvial origin and were classified by Luttmerding (1981) as silty clay loam-textured Orthic Gleysol (typic haplaquept) of the Crescent series. The top 3 cm of the soil was removed and discarded because of a surface crust and algal growth, and soil was collected from one spot to a depth of 15 cm. In the laboratory the soil was partly dried and then sufficiently crushed to pass a 5-mm seive.
4. Clover used in the column experiment
a. Production of clover
Red clover (Trifolium prat ense L.) was grown from seed in the greenhouse. The soil medium used consisted of a sterilized greenhouse soil-turfacef mix (1:1); this medium was inoculated with rhizobium but no nutrients were added.
fturface: baked montmorillonite clay. Trademark of IMC-IMCORE, Munde.lein, 111. TRANSPORT OF SOIL / 70
After 81 days the clover was harvested by washing soil and turface from the roots. Only plants that did not show flowering stems were collected to reduce variability in palatability. The plants were separated in 22 bundles and sub-samples were taken of shoots and roots for wet weight and dry weight determinations.
Six bundles of fresh plant material were then put in a 1:4 dilution of Long-Ashton nutrient solution and the roots were aerated overnight. These plants were used for the 1"C labelling. The remainder of the plant material was stored in the freezer until used in the experiment.
b. Radiolabelling of clover
In a sealed plexiglass box, the fresh plants were exposed to
-1 one pulse of 2000 jig.g C02 from Na2C03 containing 250 nCi
1 1 from NaH "C03 (110 /xCi.g" ). The radiolabeled NaHC03 was
dissolved in 5 mL of an alkaline 0.5 M solution of Na2C03.
This solution was then injected through a membrane-covered
port into a beaker suspended in the plexiglass box. The C02 was liberated through injection of 5 mL of a 4 N solution of
HCl. To stir the solution, 5 mL of distilled water was
injected with force. A small battery-powered fan circulated
the air in the box (See Appendix 2-A). TRANSPORT OF SOIL / 71
After 10 minutes an initial air sample was taken by pulling
5 mL of air into a syringe filled with 5 mL of a 10 % KOH solution. After shaking for 20 seconds, the solution was put into a vial and a 1-mL aliquot was taken and added to 9 mL of ACSf scintillation fluid. The sample was then counted in a scintillation counter.
After the sample was taken, lights (500 Watts) were switched on for 8 hours and further air samples were taken every 30 minutes. Lights were not applied during the night. The next
morning, 10 mL of the Na2C03 solution and 10 mL of the HCI solution were injected into the beaker and after four hours under lights, the box was aerated by pulling the air through
1 a 10 % KOH solution to catch any surplus "C02. All plant material was then stored in the freezer before use.
5. Experimental Set-up
The transport of organic matter into the soil profile was studied using a column experiment. In a plastic tent (6 mil polyethelene) inside an incubator, columns were set-up, made from ABS plastic sewer pipe (10 cm diameter) and closed and sealed at the bottom with an ABS plastic cap. The cap had an outlet and was connected to an overflow unit with teflon tubing. With the overflow unit, the water table was fTrademark of Amersham Ltd., Chicago. TRANSPORT OF SOIL / 72 established at 1 cm below the surface of a 3 cm thick layer of sand (0.25 - 1 mm) that was used as an unconsolidated porous plate in the bottom of the column. The water table was kept constant by means of a peristaltic pump, circulating water to the overflow unit (Appendix 2-B). On top of the sand, 30 cm of soil of the Crescent series was placed. The columns were capped with 500 mL plastic beakers.
Each of these beakers had an open air inlet and an outlet
connected to a C02 trap and air was drawn through the system with an aspirator.
After the soil in the columns was sufficiently wetted to field capacity, 8 g (wet weight) of previously frozen root material was placed in each column, covered with 5 cm of soil and then previously frozen clover shoot material (12 g wet weight) and five earthworms were added to each column.
The columns were recapped and sealed with petroleum jelly and the tent was sealed with tape. The temperature was kept at 10 °C and a 10 hour light regimen was imposed. At the end of the 30 days incubation period, all columns were stored in a freezer.
Three treatments were used: six columns with labelled shoot litter and non-labelled root litter, six columns with non-labelled shoot litter and labelled root litter and six TRANSPORT OF SOIL / 73 controls with neither material labelled. The columns in all three treatments contained earthworms. To deal with the microbial decomposition of the clover materials, two columns were added to each of the two treatments with labelled materials. These "system controls" did not contain earthworms. One column containing non-labelled litter, was equipped with tensiometers at 4, 14 and 24 cm soil depth to measure soil water potentials in the soil column.
6. Experimental design and statistics
a. Experimental design
The experimental design was a split-plot design, where the whole plots (columns) were completely randomized and two samples per plot were taken. The six sampling depths represented the sub-plot effect.
Three treatments (labelled shoots, labelled roots, control), six replicates (blocks per treatment) and two samples per block (halves of column) were chosen to maximize the sub-plot (depth) effects and minimize the block effects. A total of 36 samples of six depths each ( L, 0-5, 5-10,
10-15, 15-20 , 20+ cm) were taken. TRANSPORT OF SOIL / 74 b. Statistics
One way analysis of variance was used to describe depth effects. When it was not possible to do an analysis of variance due to incomplete data sets (dpm in cast, percent carbon), the equality of means was tested with a
Kruskal-Wallis K-sample test, while means were separated with a Mann-Whitney U-test (Siegel, 1980).
7. Sample preparation
Before sorting through the columns, they were removed from the freezer (-25 °C) and stored overnight in a refigerator
(+4 °C). The partly thawed soil columns were then pushed out of the plastic containers, split length-wise and the cast was sorted out from each of five depth layers and the litter layer. Air-dried casts were resorted and only particles that were positively recognized as casts, were included in the samples. Casts and the remains of the plants were then oven-dried (65 °C) and weighed.
For the chemical analysis, casts and soil were crushed with mortar and pestle to pass a 1 mm seive. Plant materials were crumbled by hand. TRANSPORT OF SOIL / 75
8. Chemical Analysis
The C02 traps, 250 ml erlemeyer flasks with a long and a short glass tube (4 mm inside diameter) inserted through holes drilled in a rubber stopper, were filled with 100 mL of a 0.1 N KOH solution and were changed every three to four days. A 1 mL aliquot was taken from each trap and added to
10 mL of scintillation fluid and the activity was
determined. In non-labelled controls, total C02 was determined by titration of a 25 mL aliquot with 0.1015 M HCl
with phenolphthalein as indicator. An excess of BaCl2 was used to stabilize the carbonates. The total carbon and the labelled carbon were determined with a method derived from
Snyder and Trofymo (1984) and Coughtrey et al. (1986). In modified culture tubes (Snyder and Trofymo, 1984), soil, plant and worm samples were digested in a
H2SOa-H3POtt-K2Cr207 mixture and carbon dioxide was trapped
in 3 mL of a 2 M NaOH + 0.2 M Na2C03 solution (Coughtrey et al., 1986). A 1 mL aliquot was taken from the trapping solution and was added to 1 mL NCSf solubilizer and after vigorous shaking, mixed with 10 mL OCSf scintillation cocktail. The activity was determined in a Packard LCS 4530 scintillation counter, using internal standards and automatic efficiency control. Another 1 mL aliquot was transferred to a reagent tube and titrated with 1.226 M HCl.
•(•Trademark of Amersham Ltd. TRANSPORT OF SOIL / 76
For this titration, 3 mL of a 1 M BaCl2 solution was added to stabilize the carbonates and phenolphthalein was used as an indicator.
B. RESULTS AND DISCUSSION
1. Production of clover
At the time of harvest (after 81 days), clover plants were fully grown and some had developed flowering stems. Only plants without flowering stems were collected. The average shoot weight was 0.88 ± 0.450 g (dwt, SD, n = 13), with a dry matter content of 14.75 ± 1.65 %. The average root weight was 0.146 ± 0.066 g (dwt, n = 13) with 7.9 ± 1.12 % dry matter. The shoot to root ratio was 6.03.
14 2. C02 fumigation of the clover
Approximately 360 g of fresh plants were placed in a sealed
52.6-L plexiglass box and 1"Carbon was added. After 210
minutes under 500-watt lights, virtually all labeled C02 was absorbed by the plants, No decrease in radioactivity (dpm) could be detected afterwards (Table 13). Overnight, an
increase of activity was observed as plants respired C02 under low light conditions. TRANSPORT OF SOIL / 77
Table 13. 1"C Activity in air samples measured during
the fumigation of clover plants with labelled C02.
Time (min) dpm per sample
0 61 20
30 1823
60 214
90 1 15
1 50 92
210 71
330 67
Overnight 1141
3. Observations on materials and techniques used in the
column experiment.
a. Micro-arthropods in the soil
Tullgren-funnels (10 cm screen, variable light 25 - 100
Watts; Edwards and Fletcher, 1971) were used to extract the
soil before it was placed in the columns. The extractions
did not reveal any micro-arthropods. Micro-arthropods would
have caused errors in the results by ingesting and
transporting labelled material. Partially drying, crushing TRANSPORT OF SOIL / 78 and sieving the soil eliminated all living micro-arthropods.
No extraction was done when the experiment was finished because the columns were immediately stored in the freezer.
b. Plant material
Discarding most of the stem material, only tops of plants and the complete roots were used as food in the columns. The dry matter content of the plant tops was 15.5 %, that of the roots 7.9 %.
In the columns, 8 g of root material and 12 g (wet weight) of shoot material was used, equivalent to 0.8 and 2.4 t.ha"1
(dwt) respectively. The calculated shoot to root ratio of the materials used in the columns was 3, about half of that of the young, fast growing plants in the greenhouse.
The amount of shoot material is close to the equivalent of one cut of clover hay in a four cut clover management system
(Russell, 1977).
c. Experimental temperature and soil moisture content
The experimental temperature, the high moisture content and the short light regimen would reflect spring or fall conditions in the Lower Fraser Valley. In the field, earthworms were very active under these conditions. TRANSPORT OF SOIL / 79 d. Diffusion method for carbon analysis
The determination of carbon with the "diffusion method", gave higher results than those obtained with the Leco carbon method. During the digestion, the trapping solutions in the diffusion tubes tended to evaporate, as mentioned by
Coughtrey et al., (1986). Snyder and Trofymo (1984) directly titrated the trapping solution without taking sub-samples and did not encounter these problems. Using a correction factor based on results from a standard soil (as was done in the reported experiments) measuring the volume of the trapping fluid before taking sub-samples, as was suggested by Coughtrey et al. (1986) or bringing the solution up to volume, will correct this difference.
4. Airflow above the columns
In order to remove C02 from the columns the total airflow was aimed at 600 mL.min"1. The actual flow ranged between
400 and 700 mL.min"1, because of fluctuating tap water pressures. An aspirator was used to create suction. The flow through the beakers closing the columns, was approximately
27 mL.minute-1, creating an air-change every 37 minutes in the 500 mL above the columns. This flow was sufficient to
prevent a build-up of C02. All air was drawn from inside the tent, creating an air-change in the tent every 14 hours. TRANSPORT OF SOIL / 80
5. Soil water potentials in the columns
Before the earthworms were introduced, the columns were equilibrated with water for 6 days. During this period, the pressure potential increased to -0.8 m of water. The soil reached a steady state 9 days after introducing the earthworms, as can be seen in Figure 7. The fluctuations in soil water potential in the soil near the surface, might have been caused by changes in the flow of air through the beaker, that capped the column. The humidity inside the incubator was kept at 50 %, while the air above the soil may have been saturated. The air drawn through the system was
not C02 free, therefore the variation in C02 trapped from columns may indicate a changing airflow. In column 15, with
tensiometers, high amounts of C02 trapped, indicating a high airflow, coincided with low tensiometer readings, indicating a high evaporation rate during these periods.
6. Recovery of 1"C activity from the samples
a. Specific activity of the recovered materials
Specific activities (AtCi.g"1 of carbon) of all major components are listed in Table 14. Worms fed on labelled roots showed a lower specific activity than those fed on labelled shoots. This difference in activity between roots and shoots was also noted in the recoverd cast. A large drop TRANSPORT OF SOIL / 81
cm of wottr
Figure 7. Pressure potentials at different times, in the soil column during the incubation of earthworms (10 °C). TRANSPORT OF SOIL / 82
Table 14. Specific activities (yCi.g~1Carbon) of materials recovered from the soil columns.
Labelled roots Labelled shoots
Cast 0.0304 0.562
Worms 0.0264 2.68
Litter before 3.23 3.67
Litter after 0. 1 52 3.24
Av. Littert- 0.630 3.46
t-Average litter value is calculated from 'litter before' and 'litter after', using a weighted average, based on the evolution curves in Figure 8.
in specific activity was found in root material over the
course of the experiment. The high lignin content of the
root material and the leaching of carbohydrates from this material may have caused this drop in specific activity. In
1 pulse-labelling experiments with *C02, most of the carbon
is incorporated in mobile carbohydrates and not in
structural components of the plants. TRANSPORT OF SOIL / 83 b. Total activity of recovered materials
The calculated total activity in the plant materials, used in the column experiment was 30.95 MCi. At the end of the experiment 20.77 uCi could be accounted for (Table 15).
Losses may be caused by the contamination of the bulk soil, inefficiency in sorting the casts from the columns and
1 losses of "C02 during sorting and storage. Inefficiency in sorting may lead to an under-estimation of the egestion
1 rate. Losses of "C02 during storage may affect equally shoot or root materials, because the largest losses take place in the early stages of the experiment. No effect on the shoot to root ratio in the earthworm diet is to be expected due to losses of activity from plant materials.
c. 1"C activity recovered from the bulk soil
Labelled shoots caused a slight increase of activity above background levels in the soil layers immediately below the surface. Above the labelled roots however, a very significant increase in activity was noted (739 dpm.g"1 soil), most likely caused by the upward movement of moisture and gases in the column. In the field, normally a down flow of water takes place. Carbohydrates and other components, exuded by plants may move down into the profile with the water. The downward movement of radio-labelled components
1 exuded by plants that were treated with "C02 in the field, TRANSPORT OF SOIL / 84
Table 15. Total 1*C activity recovered from materials in the soil columns.
Source //Ci
In Shoots 23.58
Roots 7.37
Total in 30.95
Out Respiration 8.86
Cast roots 0.09
Cast shoots 1 .88
Worm roots 0.03
Worm shoots 2.65
Roots 0.14
Shoots 3.01
Roots blank 0.06
Shoots blank 2.00
Soil roots 1 .07
Soil shoots 0.98
Total out 20.77 TRANSPORT OF SOIL / 85 was described by Dietz and Bottner (1981). The components could be detected by radiography in the top 5 cm of the mineral soil. Casts collected from the surface were not affected by this contamination (344 dpm.g"1 cast), but the cast recovered from the soil layers may have been affected,
because large differences in activity between the cast from
the surface and from the soil layers were found. A correction was made in the activity by subtracting 739 dpm,
before the calculations were done to estimate the use of
roots and shoots by earthworms. Further discussion of the difference in levels of 1ttC activity is found in section 11
b.
7. Respiration and decomposition
a. Respiration
1i, Column respiration, expressed as trapped C02, showed a
high variability within each treatment group, but the
variation was related to each column. This variability may
be explained by the position of the plants in the fumigation
box. Plants at the side of the light source might fix more
C02 than those in the shade. Plants were not mixed before
being used in the columns. Also soil packing might have
caused variability. When measured activity counts were
related to those of the first sampling date, and expressed TRANSPORT OF SOIL / 86
IOO -
%
50 -
3 6 9 13 16 20 23 27 30
DAYS
Figure 8. Decrease in 1,C activity (% first measurement,
SD) of C02 released through respiration. TRANSPORT OF SOIL / 87 as a percentage, the variability was reduced (See Figure 8).
The evolution rate of '"COj, expressed in average activity per day, varied from approximately 15000 dpm at day 3 to
1724 dpm at day 30 for columns with labelled leaves and from
1600 to 210 dpm for columns with labelled roots. The largest drop in evolved activity occurred during the first few days
of the experiment. A total of 8.84 uCi was recovered. The
background for this stage of the experiment was 35.8 ± 6.17 dpm (n=22)
The trapped C02 and the recovered activity from columns used
as system controls (no worms added) were not significantly
different from the treatments. The earthworms did not have a
1U noticeable effect on the rate of C02 evolution, probably
because the 1*C activity was confined to mobile
carbohydrates. In a pulse-labelling experiment, only a
1tt limited amount of C02 is incorporated in the structural
components of plants. These mobile carbohydrates, sugars
etc., are easily assimilated by microorganisms inhabiting
the plant material. The decomposition of structural
components in later stages of the decomposition process, may
be affected by shredding and mixing by earthworms and by the
proliferation of fungi and bacteria caused by earthworms.
(Shaw and Pawluk, 1986). Earthworms may not have a TRANSPORT OF SOIL / 88 significant effect on the decomposition of organic matter in the early stages of decomposition.
b. Weight loss of clover material
Shoot material lost 56 % of its original weight in the columns without worms over the duration of the experiment, probably due to non-faunal decomposition and other processes. Root materials lost only 6.9 % of their weight.
The constant temperature and high humidity in the columns, may have aided the decomposition processes. Weight loss during the decomposition of clover plants was described by
Uvarov (1982). He found a weight loss of 60 % during the first year. Uvarov (1982) cited several studies, reporting weight losses from clover stems and leaves as high as 61 %, over a period of 2 to 3.5 months. Thus the high weight losses during the 30 days of the experiment may not be unusual.
The 1 *C activity in casts recovered from columns with labelled shoot material was substantially higher than that in cast from columns with labelled root material, while the specific activities of both shoots and roots were similar at the start of the experiment. Differences in ingestion rate and a different decomposition pattern of roots may explain this difference. For shoots, the decomposition of soft TRANSPORT OF SOIL / 89 materials and a breakdown of simple carbohydrates takes place simultaneously; the specific activity stays constant.
Roots, however, have a rigid structure and simple carbohydrates are leached from this material before a substantial weight loss is seen from the breakdown of cellulose and lignin. Malone and Reichle (1973) demonstrated this clearly when they followed labelled cesium during the decomposition of root material. The cesium was lost from the
roots much faster than the loss of biomass would indicate.
8. Recovery of casts from the soil columns
a. Description of the burrows
Cast particles that could be recovered, were removed from
the surface of each column. The partly frozen soil was then pressed out of the plastic columns. In the 0-5 cm layer, the burrow walls (all cast material) were thick and easy to
recognize and recover. Some of the burrows were blocked with cast aggregates. Along the sides of the columns, the worms had created "reinforced" burrows made of large amounts of casts. In the 5-10 cm layer, the burrow walls were not very
thick but could easily be removed by peeling material from
the surrounding soil. The 10-15 cm layer, and those below, contained burrows along the sides of the column. The soil at
the sides of the column might have been less packed, TRANSPORT OF SOIL / 90 increasing aeration and penetrability and was thus more accessable to earthworms. This border effect and the optimum diameter of columns should be examined more closely. These burrows along the sides of the column had very thin walls with virtually no recoverable casts and some burrows showed only slightly smeared tracks. The small amounts of casts recovered from these burrows may indicate that the worms did not use them often. In several columns, worms were recovered from these deep burrows. Disturbance due to the discontinuation of the experiment and the transport of the columns might have caused an escape reaction forcing the worms down. The burrows with thin walls, might have been dug during the first few days of the experiment as part of a panic or escape reaction as discussed for A. rosea by
Phillipson and Bolton (1976). No reports were found to confirm this behaviour of L. rubellus. In the field it was noted that the worms pull into their burrows when they were disturbed.
Burrows were found in the soil mass close to the water table. Due to the high soil water content, the burrow walls were smeared and no cast could be recovered. These deep burrows might indicate that a high soil water potential is not a restricting factor in the burrowing depth of L. rubellus. The water table itself, anaerobic conditions or TRANSPORT OF SOIL / 91
toxic gas (H2S) may be the regulating factors.
b. Description of casts
Casts were relatively easy to recover because of their compact structure, irregular rounded and indented shapes, their colour (Munsell: 5Y, 3/2, dark olive green or darker, when wet), the high amount of fibres in them and the lack of mottles inside broken-up aggregates.
The bulk soil was of a loose structure, with blocky aggregates with sharp edges. The colour was lighter than that of the casts and less green (2.5Y 4/2, dark greyish brown, when wet) and not many fibres were visible.
9. Distribution of casts
The average amount of cast recovered from each column was
34.28 ± 3.85 g (n=l8). Columns from which less than 5 worms were recovered (10 % mortality was observed), showed a cast production that was slightly less than the average (27.48 ±
4.66 g, n=8). Because the mortality occured systematically in all treatments no distinction was made regarding the recovery of worms. (Control = 30.76 ± 8.15; Leaves labelled
= 32.63 ± 2.94; Roots labelled = 30.38 ± 4.42 g, SD, n=6).
Few casts were found in the 20+ cm layer, the bulk was found in 0-5 and 5-10 cm layers. The distribution of total cast TRANSPORT OF SOIL / 92
Table 16. F-values for contrasts of total cast, recovered from columns, after incubating earthworms with labelled clover shoot or root material added. Total cast recovered; the linear test was performed first (** p > .99, * p > .95); SS = sum of squares, MS = mean square).
ANALYSIS OF VARIANCE - CAST
Source o4 variation cH F SS MS
Treatment (T) 2 0. 35 1.B60 0. 940 Control vs T k B (Tl) 1 0.05 0. 13B 0. 138 Top vs. Bottom (T2) 1 0.64 1.742 1. 742 Pot/T - Error (a) 15 0.54 40.B14 2. 721 Core/P/T - Error (b) IB 1.60 90.270 5.01 5 Depth (D) 5 B0. 84 ** 1264.835 . 252.96 7 Litter/other (DO) 1 1.27 3.960 3. 9B0 Linear (DI) 1 363.01 ** 1135.937 1135. 937 Guadratic (D2) 1 39. B9 ** 124.641 124. 841 Residual A. 0.01 0.076 0. 039 Treatment X Depth (TD) 10 1.64 51.461 5. 146 Tl X DO 1 0. 10 0.316 0. 316 Tl X DI 1 7.98 ft 24.971 24. 971 Tl X D2 1 6.77 * 21.182 21. 182 T2 X DO 1 0.00 0.001 0. 001 T2 X DI 1 0.59 1.B34 1. 834 T2 X D2 1 0. 20 0. 632 0. 632 Residual 4 0. 20 2.524 0. 631 D X P / T - Error (c) 75 1.41 234.693 3. 129 D X C /P/T - Error
The order of testing the polynomials appeared important: when the linear test was performed first, 90 % of the variability could be explained with a linear equation, when the quadratic test was done first, 85 % of the variability was attributed to a quadratic curve. Because the second test is done on the residual of the first one, the description of the curves depends on the sequence of testing (Eaton, personal communication).
10. Egestion rates
The egestion rate of L. rubellui was 2.34 g.g"May"1, calculated for columns from which 5 worms were recovered.
The average dry weight of the earthworms, measured before the experiment, was 0.094 ± 0.0238 g (n=13). The egestion rate calculated from the column experiment is close to the results reported by Martin (1982) for the egestion of soil and grass meal (not converted to dry weight basis). The egestion rate in the column experiment was higher than was TRANSPORT OF SOIL / 94
CM 0
10
I 5
20
25
20 30 40 50 % total cast
Figure 9. Distribution of cast ( % of total cast per column, SD) according to depth. TRANSPORT OF SOIL / 95 found in the litterbag technique (Chapter III) and was well above figures found in the literature for L. rubellus (see also Table 10). Different food or different experimental conditions (temperature and moisture) may have caused the these differences in egestion rate. Further discussion may be found in section 11 c.
Using a weighted average for the percent carbon in cast as related to depth, a total of 46.13 mg.g"1.day1 carbon was egested by the worms. No information was found in the literature on the egestion rate of carbon for L. rubellus or any other species.
11. Organic matter
a. Distribution of organic carbon in the cast
Organic matter was redistributed in the soil profile by the worms in two ways: through ingestion and casting and through physically pulling material into the burrows. The percentage of carbon in the cast indicates the amount of organic matter ingested by the worms. The carbon content of the cast was higher than that of the ingested soil (1.8 % vs. 1.24 %), but no significant decreasing trend with depth was found
(Kruskal-Wallis K-Sample test, Figure 10). TRANSPORT OF SOIL / 96
1
litter layer —4 j !
—, • 1
"o i
CO 1 1 1 1 10 20 %C
Figure 10. Distribution of Carbon (% Carbon, SD) in cast according to depth. TRANSPORT OF SOIL / 97
b. 1I|C activity in casts as related to depth
•For shoots no significant decrease in 1*C activity was noted
in the cast related to the depth. A large variability (50 %)
was found in the 1"C activity in these casts. This large
variability could be explained by the non-homogenized
labelled plant materials used in the columns as earthworm
food.
Casts from columns with labelled roots, showed a different
pattern. Casts found on the surface of the soil had a low
activity (344 ± 29.5 dpm.g-1 cast, dwt), while cast in the
soil layers was much higher (> 1000 dpm.g-1) with large
variability (80 %). A non-significant decrease in activity
with depth was found. The contamination of the bulk soil
above the root-litter layer (approximately 700 dpm.g"1), may
be proof of the rapid assimilation of mobile carbohydrates
by microorganisms. The relatively high contamination in the
bulk soi] may also have influenced the level of activity in
the sub-surface cast. These carbohydrates were leached from
the root material, as was discussed in 7 b. No contamination
of the bulk soil was seen in columns with labelled shoots
and the activity of surface cast was not lower than that of
sub-surface cast. The 1<4C activity in the cast in these
columns was two orders of magnitude higher than in cast in
columns with labelled roots. TRANSPORT OF SOIL / 98 c. Calculation of the use of added organic matter by the earthworms
Shoot material was almost completely removed from the surface of the soil, while most of the root material was not moved. In the zone where the roots were buried, horizontal burrows were found, but the root material itself was consumed only slightly by the worms, indicating a low palatability of the root material or a lack of a microorganism population on the material. Either cause may be supported by the fact that mobile carbohydrates leach from the roots in the early stages of the decomposition process. Invasion by lignin decomposer populations may take longer than the 30 days the experiment lasted.
After the decomposition weight-loss was subtracted from the original amount of litter, approximately 15.4 % of the shoot material, mostly stems, was recovered from the columns with wovms. About 73 % of the roots were recovered, the loss by decomposition was minimal (6.9 %). Based on these ingestion figures, roots accounted for 17.9 % and shoots for 82.1 % of the consumption of added organic matter.
The 1"C activity measured in the recovered earthworms was used to calculate the feeding by the worms on the shoot or root materials that were added to the columns. In this TRANSPORT OF SOIL / 99 calculation, a weighted average of the evolvement of
labelled C02 was used to correct for the decrease in specific activity of the root materials during the experiment. Roots contributed 17.8 % of the added organic matter that was ingested by the worms, while shoot material accounted for 82.2 %.
Using a similar approach with the weighted average, the use of organic matter was calculated from the 1"C activity recovered from the cast materials. The calculated use of roots was slightly higher (21.8 %) and the use of shoot material was slightly lower (78.1 %) than was found in the previous calculations.
All three independent methods, the calculation from the ingestion of organic matter, from the activity in the worms and from the activity in the casts, gave similar results. In this type of column experiment, the use of added organic matter could have been estimated without the use of a radio-tracer. In experiments where the root materials are mixed into the soil, tracers are definitely an asset to estimate the relative consumption of shoots and roots by earthworms. The shoot to root ratio in the diet is valid early in the decomposition of the plant materials. The palatability of roots may increase over time, when a TRANSPORT OF SOIL / 100 decomposer population develops. On the other hand, L. rubellus is known to ingest fairly undecomposed materials.
The ratio may not change that much.
12. Testing of assumption
L. rubellus burrowed to a depth of 35 cm, was found throughout the columns, deposited only 15 % of its cast on the surface of the soil and was active in the top 15 cm of the profile where most of the cast was deposited. The worm ingested 20 % litter as root material. Based on this evidence, the assumption that L. rubellus is an epigeic worm, only feeding and casting in the litter layer, must be rejected. V. EARTHWORM SIMULATION MODELS
A. SIMULATION MODELS DESCRIBING THE DYNAMICS OF SOIL MIXING
BY EARTHWORMS
1. Introduction
Models have been used to increase the understanding of ecological systems, to predict the results of individual processes or a combination of processes or to predict the results of a single laboratory experiment. Several conceptual and simulation models have been developed for earthworms. The conceptual models describe the parameters that influence the distribution of earthworms (Reynolds and
Jordan, 1975) or the consequences of earthworm activity
(Bouche and Kretzschmar, 1977). Simulation models estimate the population growth and/or soil turn-over for a single species over a relatively short period.
2. Published earthworm models
Reynolds and Jordan (1975) developed a conceptual model to describe the distribution of earthworms. Many soil-related factors such as moisture, temperature, colour, aspect and texture were included.
101 EARTHWORM SIMULATION MODELS / 102
The consequences of earthworm activity in the soil profile were described in a conceptual model by Bouche and
Kretzschmar (1977). This model, "REAL," included population dynamics, mechanical activities of earthworms in the soil and the possible effects of worm activity on the ecosystem.
Growth and development of populations was described by the population dynamics model "MOTOMURA." This model was tested for earthworm populations across Europe by Lecordier and
Lavelle (1982). The model could be used in 80 % of all cases, but the authors rejected it because no relation could be established between the slope value in the model (the environmental constant) and any environmental factor in the field.
Reichle (1971) described a mathematical model to simulate the carbon flow in a woodland system, containing earthworms.
Carbon from five components is followed: litter 0, and 02, mineral soil, earthworm biomass and extractable earthworm
biomass. The ingestion rate was related to the Q10f the relative increase in assimilation over a 10 °C interval.
Reichle's model utilized data for Octolasium lacleum obtained by Crossley et al., (1971). A population of 14 g.irr2 ingested 208 g.nr2.y~2 of organic matter, and egested
167 g.m"2.y"2 with 40 g.irr2.y~2 being assimilated. EARTHWORM SIMULATION MODELS / 103
The model "WORM.FOR" was presented by Mitchell (1983) to
describe biomass production and food consumption by E. foetida in waste conversion systems. This model used
functions based on empirical information. The growth-rate
function was related to the growth conditions and the Q10
was included in the description of temperature effects. Four
subroutines, mortality, growth, reproduction and ingestion
were used in weekly steps to calculate biomass production
and food consumption.
Cast production of the tropical earthworm M. anomala, was
first calculated by Lavelle (1975), using a model based on
population data and earthworm activity. This model was the
basis for a simulation model "ALLEZ-LES-VERS" (Lavelle and
Meyer, 1977, 1983). The population growth was the basis of
the simulation. Soil moisture and soil temperature data were
used to calculate the turn-over of soil and organic matter,
as they both influence earthworm activity.
The simulation models presented above, describe the growth
and activity of a single species in a specific environment
during a short period. WORM.FOR dealt with E. foetida in
waste conversion systems in a simulation over 20 weeks,
ALLEZ-LES-VERS simulated the egestion of soil and the
population dynamics of M. anomala in the Lamto savanna, EARTHWORM SIMULATION MODELS / 104
Ivory Coast, during a period of a year; and Reichle's model is specific for an Eastern North American hardwood forest, also for one year. None of these simulation models estimate the long-term effects of earthworms on the soil system.
Information on long-term effects may be important for the reclamation of waste lands and in the study of "ecological agriculture" and in forest management. A soil mixing simulation model that is widely usable, is also needed to develop new hypotheses in the study of ecological processes.
3. "MIXER", a new conceptual model describing earthworm activity in soil systems
a. Introduction
Based on literature data, a new conceptual model, "MIXER," is developed, describing earthworm activity in soil systems.
This new model includes the moisture and temperature relations for L. rubellus, that were developed in Chapter
III. The model is a multi-species, non-specific model that can be used in a wide range of conditions. It is based on the morphological - functional classification as described by Bouche (1977), as well as on components from the conceptual model by Reynolds and Jordan (1975). In this model, the movement of mineral and organic matter in the soil profile is central. The model can easily be adapted for EARTHWORM SIMULATION MODELS / 105 long-term computer simulations.
b. Soil layers in the model
Earthworms react to their environment; their activity, reproduction, survival and growth are based on the environmental conditions of which moisture and temperature may be the most important (Bouche, 1984; Satchell, 1980;
Lavelle, 1975; Reynolds and Jordan, 1975). With regard to earthworm activity in the soil system, the soil profile may be separated into three layers: the organic matter or litter layer on top of the soil (I), the mineral soil layer in which most of the biological activity takes place, (II), and the subsoil (III). Because earthworms may change the pedogenic horizons in the soil profile through soil mixing
(Langmaid, 1964), terminology from the Canadian System of
Soil Classification (Canada Soil Survey Committee, 1978) is not used.
c. Population dynamics
The carrying capacity of a site will determine the population density and must therefore be included in the model. Carrying capacity is determined by the availability of food, environmental variables such as moisture, temperature, type of vegetation, drainage and soil management. Other factors are bird predation on earthworms EARTHWORM SIMULATION MODELS / 106
(Cuendet, 1983; Satchell, 1981), predation by soil vertebrates and other soil animals (Lee, 1985; Macdonald,
1983) and competition between species (Abbot, 1980; Bouche,
1977). A Site Quality Index, similar to one used in
Forestry-management, would be a useful tool to estimate maximum earthworm populations in a given site. Once the
relative carrying capacity for each worm species is
established, the recovery of the population can be predicted
after a major (man-made) disturbance (rototilling, ploughing
and seeding, harvesting, slashburning, pesticide spraying)
or after earthworm introduction or soil improvement
(drainage etc.). The growth curve first may exhibit
exponential growth, but once food or predation becomes
limiting, the growth curve flattens out, and the carrying
capacity is reached. After the growth phase, the seasonal
effects, such as temperature and drought stress, will become
obvious in the biomass. In agricultural situations, where
soil management takes place during each cropping season, or
every two to three years in longer rotations, the maximum
possible biomass may not be reached. In permanent pastures,
forested systems and possibly in lands under a
limited-tillage cropping practice, carrying capacity may be
reached.
The total population of each worm species may be divided EARTHWORM SIMULATION MODELS / 107
into proportions of young (small) worms, immature adults and mature (clitellated) adults. This is necessary because the
ingestion rate of the worms depends on their age
(Hartenstein et al., 1981; Phillipson and Bolton, 1976;
Lavelle, 1975). The relative abundance of each age group
varies according to season (Reynolds, 1976).
d. Earthworm food
Until recently, the food of earthworms was described as soil and organic matter; microorganisms are now regarded as an
important food source of earthworms, as was discussed in
Chapter II.
The quality of the food influences the amount ingested
(Lavelle , 1975; Appendix 3-B), therefore a system should be
developed to rate the quality of food based on palatability, moisture content, carbon to nitrogen ratio, etc. This Food
Quality Index could be a reflection of the decomposition
rate of organic matter (Reynolds and Jordan, 1975) or of microbiological activity. If the worms digest microorganisms
that inhabit the food material, cast material may also be an
important part of the diet as reported by Bouche et al.
(1983). The consumption of casts may be dependent on the
aging of faecal material, following nitrification and microorganism blooms, 6-7 weeks after egestion in
temperate regions (Bouche et al., in press). Bouche et al. EARTHWORM SIMULATION MODELS / 108
(1983) calculated that the anecic Nicodrilus velox ingested
50 % its carbon needs from recycled casts. The other carbon would come from the litter layer (Bouche et al. in press).
Therefore organic matter should be divided into age classes, each worm species will ingest the age class of its choice.
Ingestion of soil by some species can be seen as a method for "making up" a deficiency in food when organic matter cannot supply the amount of nutrients needed. Soil might be a reliable but "low quality" source of food, and it is required for grinding processes in the gizzard. The
ingestion of carbon, as discussed in Chapter III, may be an
important parameter, describing the energy needs of earthworms and needs to be studied as a basis of food-intake behavior.
The consumption patterns of earthworms with different strategies will vary. The following feeding patterns are arbitrarily established. Epigeic species: 100 % from layer I
(L); endogeic species: 100 % from layer II (Ah); and anecic species: 70 % from layer 1,10 % from the II (Ah) and 20 %
from layer III (BC). EARTHWORM SIMULATION MODELS / 109 e. Cast production
A worm population that consists of several species with different strategies, will be the most effective in mixing
soil and incorporating organic matter. Cast production and
the soil layer in which casts are produced are species
specific. The following pattern of cast production is arbitrarily established: epigeic species: 100 % in layer I ;
surface casting endogeic species: 90 % in layer I, 10 % in
the II; sub-surface casting endogeic species, 10 % in layer
I, 90 % in II; and anecic species: 100 % in layer I.
f. Flow-diagram for MIXER
The flow-diagram of the proposed conceptual model is shown
in Figure 11. The worm compartment contains the population
growth parameters and the species differentiation, as well as basic ingestion information. Site Quality (climate,
nutrition, plant community, soil type, succession) directly
influences the abundance of species at the site. The food
intake of each species or group of species, depends on the
temperature and moisture fluctuations in the soil and on the quality of food available. The amount of food ingested
depends on the age of the worms, immature worms ingest
relatively more material than clitellated adults.
In the soil compartment, the sources of food and the EARTHWORM SIMULATION MODELS / 110
abundance biomass by species by age
gut conte nt
0-
plant
Figure 11 . Flow diagram for the earthworm model MIXER.
I = Litter layer, II = Upper soil layer with most of the biological activity, III = Subsoil, CH = Choice of food, G = Population growth, E = Egestion rate, In = Ingestion rate, M = Moisture effect, OM = Organic Matter, SQ = Site Quality, T = Temperature effect. The squares indicate different age of mater ial. EARTHWORM SIMULATION MODELS / 111 distribution of cast are described; included is ingestion of litter, cast and soil from the different soil layers. Worms ingest soil and organic matter from different layers in the profile, according to their strategy. As earthworms ingest plant material that is sufficiently decomposed to their taste, a cohort system for litter is included in the model.
Each new batch of plant litter added to the soil, is followed over time, till the required state of decomposition is reached. This cohort system for plant litter also enables the researcher to model competition between species with different preferences for litter. Cast is deposited in the soil system at a depth, specified for each worm species or strategy. By using different coefficients for the intake of certain food materials, several ingestion patterns can be simulated. Assimilation and excretion of mucus and urine is not included in the model although Bouche et al. (in press) described the importance of earthworm excretions to plants.
B. F-MIXER, A SIMULATION MODEL FOR SOIL MIXING BY EARTHWORMS
1. Introduction
The conceptual model MIXER, which includes the results of the moisture and temperature experiments, and the results of the 1"C column experiment were used to create a model for the simulation of movement of mineral and organic matter EARTHWORM SIMULATION MODELS / 112 into the soil profile.
In the discussion of MIXER, emphasis was given to the distribution of cast in the profile and the intake of food.
The column experiment, described in Chapter IV, resulted in information on the distribution of cast in the profile by L. rubellus and its choice of organic matter. The column experiment itself is used as an integral part of the computer simulation version of MIXER.
The objectives for creating the simulation model were a) to test the understanding and knowledge of soil mixing by earthworms, b) to extrapolate the data from the column experiment and c) to provide the ecosystem modeling framework, "FORCYTE," with a soil mixing component.
FORCYTE was choosen as the model to carry MIXER for three reasons. First this ecosystem model lacked a soil mixing component; secondly because FORCYTE is a long-term trend analysis model and thirdly because MIXER could be included with a minimal amount of programming. Modification of
FORCYTE to fit the requirements of an agricultural ecosystem model, which would simulate crop production and the effects of crop management, will require substantially less time and effort than building and programming a separate model. The EARTHWORM SIMULATION MODELS / 113 simulation version of MIXER was therefore written as a sub-routine for a forestry model. This soil mixing model is suited to simulate earthworm activity in both agricultural and forested systems..
2. A brief description of FORCYTE
The model FORCYTE (FORest nutrient Cycling and Yield Trend
Evaluator) is a very large and complex model that evolved over several years to become an ecological modeling
framework. In this respect, it can be used, after suitable calibrations, to model plant production in any ecosystem.
FORCYTE is not sensitive to seasonal fluctuations in environmental conditions, but will analyse trends in production levels over several decades. The simulation for
forested systems is done for up to three crop rotations (240 years).
The most recent version of FORCYTE, FORCYTE-11, is a hybrid
stand - individual tree growth model, based on historical
yield data and ecological processes of either managed or
unmanaged forests. The model examines, on an ecosystem-type
basis, the change over time in community composition, the
production and biomass of mosses, herbs, shrubs and trees,
the nutrient budget and nutrient circulation for up to five
nutrients, the inventory and dynamics of organic matter, and EARTHWORM SIMULATION MODELS / 114 the economics of production management (Kimmins, 1986;
Kimmins et al., 1981). The soil part of the "SETUP" program of FORCYTE consists of "SOILDATA," the input file,
"FORSOIL," the simulation part and several output files.
These output files are used in "FORCASTER" to simulate management regimens. The results of FORCASTER and FORSOIL are graphed and tabulated.
The simulation of the SETUP program to aquire data to run
FORCASTER, is based on the simulation of short-term experiments, that can easily be done in the laboratory or as field experiments. Examples are sorption and desorption experiments, decomposition trials, etc. To include soil mixing by soil invertebrates as a sub-routine in FORCYTE, the column experiment from Chapter IV was used as a short-term experiment in SETUP to generate empirical data on the redistribution of soil and organic matter. For each earthworm species or group of species with similar strategies, a column experiment is needed to calibrate the model (i.e., epigics, etc.).
3. Description of the FORCYTE version of MIXER
The FORCYTE version of MIXER (F-MIXER) has been developed from the conceptual model to fit the requirements of
FORCYTE. To obtain information on soil mixing by earthworms, EARTHWORM SIMULATION MODELS / 115 a column experiment is simulated, using soil and organic matter as well as the average soil moisture and soil temperature of a site. In each time step (one year), a specific amount of root and shoot litter is added to the columns and the worm population is kept constant. The availability of carbon to the worms will check their consumption of soil and organic matter. A maximum ingestion rate may be specified for each worm type. Worms in F-MIXER proportionally ingest organic matter from each soil layer, mix it with soil to form cast and deposit the cast proportionally in the layers. Fluctuations in moisture and temperature status of the soil are averaged and are kept constant. The organic matter used in the simulation is of palatable quality and is aged to fit the worms' taste.
Cast produced in a soil layer is classified as humus after each year (one time step) and may be recycled by earthworms.
As cast is reclassified as humus, nutrients in excess of those specified for humus are released. These nutrients are used in FORCASTER to affect plant growth and influence crop production predictions. Appendix 6 shows a detailed description of the processes and data requirements for
F-MIXER. EARTHWORM SIMULATION MODELS / 116
4. Comparison of F-MIXER to MIXER
The results from a simulation of crop production or earthworm mixing using an ecosystem model, may not reflect the actual future state of the simulated ecosystem. F-MIXER was designed to evaluate trends based on the available knowledge of the processes shaping ecosystems, not as a model to predict exact quantities of mineral soil and organic matter cycled or to fit the results of a short-term exper iment.
The conceptual model MIXER as presented before, is different in several ways from the presented F-MIXER. MIXER requires detailed information on the soil temperature and moisture regimens at a certain site for a short-term evaluation.
Under Lower Mainland, British Columbia, conditions, the influence of drought on the earthworm activity is minimal, as can be seen from the data presented in Appendix 5. The yearly temperature fluctuation, however, was seen in the calculated monthly cast production. Assuming a fluctuating temperature has the same effect on the egestion rate as the the average temperature, calculated from these fluctuations, no detailed information on soil temperature is needed for long-term simulations. The effects of climate on crop production are covered in FORCYTE by using yield curves and EARTHWORM SIMULATION MODELS / 117 the concept of biogeoclimatic zones. The yield curve includes the effects of climate and other site-specific parameters on the growth of plants. No similar information is available for earthworms, and no data were found regarding the effects of fluctuating temperatures on the egestion of soil by earthworms. Reinecke and Kriel (1981) reported a lower cocoon production for Eisenia foetida in earthworms incubated at a fluctuating temperature with an average of 20 °C, compared to a constant temperature of
20 °C. Differences in cocoon production were not found for
10, 15> and 25 °C. The topic of the effect of temperatures, fluctuating or constant, on earthworm activity, needs more study.
To include detailed information on worm age-classes and moisture and temperature effects, a different type of simulation model should be developed. This model may not simulate the long-term trends in the soil system, but will describe the short-term effects of an earthworm population.
Such a model would be a population or production based model, similar to ALLEZ-LES-VERS (Lavelle and Meyer, 1978) or WORM.FOR (Mitchell, 1983).
In long-term simulations, the age structure of the earthworm population may not be needed, although the egestion rate for EARTHWORM SIMULATION MODELS / 118 the total population should be calibrated to include the higher egestion rates of young specimens. Population density changes, as influenced by available food, should be incorporated into the model.
5. Simulation
The biological functions of F-MIXER were tested with the simulation of the transport of mineral soil and organic matter in an agricultural system. In this system, a no-tillage management concept was assumed. A series of crops was followed over a 45 year period. After each growing season, crop residue was left on the surface. The palatability of this residue for earthworms was assumed to be similar to that of clover material, decomposition rates for clover were used: 60 % weight loss during the first year for shoot material (Uvarov,1982) and 20 % for roots.
Earthworm biomass at several levels (0, 50, 100, 200 and 590 kg.ha"1, dwt) were used to simulate the organic matter and mineral soil transport in the profile. Enrichment and depletion of organic matter was followed in the litter layer
(I) , the upper mineral soil layer with earthworm activity
(II) and a sub soil layer (III).
An earthworm biomass of 590 kg.ha"1 (dwt) could not be supplied with enough surface litter (Figure 12-A). This high EARTHWORM SIMULATION MODELS / 119 level (590) chosen for the column experiment to obtain significant casting in a short time, may not be realistic under field conditions. All surface litter was ingested and redistributed into the profile. The exhaustion of surface litter was expected because the worms removed nearly all the shoot litter during the 30 days incubation in the column experiment. At a level of 200 kg.ha"1 (dwt), the worms just removed all the litter that was supplied each year, and mixed it into layer II.
The curves in Figure 12-B, describing the organic matter content of that layer, show an increase in organic matter over time. The curves for the two highest populations indicate similar levels of organic matter and show that there is no further increase in organic matter possible, once the litter layer is consumed.
Because in the model, the worms indiscriminately ingested a mixture of root material, mineral soil and humus, contrary to the results of the column experiments described in
Chapter IV, their population should have been limited by the maximum intake of organic matter. Earthworm biomass between
200 and 250 kg.ha"1 as found in the Lower Mainland (see
Appendix 2-D) and in a no-till situation in Georgia EARTHWORM SIMULATION MODELS / 120
(Parmeleet, personal communication), are more realistic.
Mechanisms in the model to actually link population densities with available organic matter and to model preferential feeding on root materials, are currently being developed.
The curve for the highest worm density (590) in Figure 12-B is lower than that for 200 because of recycling of organic matter and the decomposition of these recycled materials.
The percent organic matter in layer II without worms, decreased slightly over time due to decomposition.
Large amounts of soil were ingested by the worms. The soil intake of the 200 kg.ha-1 worm population, ranged from 48 to
111 t.ha"1 (Figure 12-C), well within the range of published figures for surface cast in temperate regions (4.5 - 90.2 t.ha'1). The worms need to process a certain amount of organic matter to survive (46 mg.g-1.day"1 of carbon at 10
°C in a soil at field capacity). In the model the worms get this amount by ingesting surface litter and soil: 43 % of the carbon needs from layer I, 56 % from II and 1 % from
III. These values were calculated from the organic matter intake in the column experiment. When the earthworms add organic matter to the pool in layer II, by ingesting surface f R~. Parmelee, Ph.D. Candidate, Institute of Ecology, University of Georgia, Athens, Georgia, USA. EARTHWORM SIMULATION MODELS / 121
0 200 t/ho 50 59 0 10 100 - -
/ y 5 / / / / / /
V
5 10 20 45 YEARS
Figure 12-A. Results of the simulation of F-MIXER, the accumulation of surface litter (t.ha'1 (dwt), as affected by earthworm populations (kg.ha"1, dwt).
20 0 %c 50 59 0 100 1 c
5
£ 10 20 45 YEARS
Figure 12-B. Results of the simulation of F-MIXER, the organic matter content (%) in layer II, as affected by earthworm populations (kg.ha-1, dwt). EARTHWORM SIMULATION MODELS / 122
50 200 1 0 0 590 t/ha
400
v.
200
100 _
5 10 20 Y EARS 45
Figure 12-C. Results of F-MIXER, the ingestion of soil (t.ha-1, dwt) by different populations of earthworms (kg.ha"'1, dwt). EARTHWORM SIMULATION MODELS / 123 litter and egest it in the mineral soil, the concentration increases and thus less of a soil-organic matter mix is needed from this layer to satisfy the carbon requirements.
The egestion of soil will therefore decrease over time. By this mechanism it is assumed that cast material is recycled by earthworms.
The movement of mineral soil from one layer to the other, through earthworm activity, caused depletion of soil in mineral soil layers or an excess of soil in the litter layer. This problem was addressed by developing a method to simulate moving soil-layer-boundaries. Starting from the lowest layer, the deficit in mineral soil was filled by transferring soil from the layer above. Surface cast is included in the upper mineral layer. The transferred soil contains an amount of humus similar to that of the soil in the receiving layer.
The humus content of the litter layer depended on the decomposition rate of the clover materials (with the last decomposition class transferred to humus) and on the accumulation of cast. The cast that was deposited on the surface of the soil by the earthworms, was transferred in the model to the mineral soil. As the transferred materials contained the humus content of the receiving mineral layer, EARTHWORM SIMULATION MODELS / 124 some humus accumulated in the litter layer. This humus was re-used by the worms feeding on the litter layer.
6. Improvements needed in F-MIXER
The worms did not achieve their maximum organic matter intake, because in the model they did not switch to another organic matter source when one is depleted. Indiscriminant ingestion of soil with roots and humus may not be a good representation of worm feeding. A correction factor or a
"hunting routine" should be included in the model. For L. rubellus the ingestion ratio between shoot litter and root litter is known (4 to 1, see Chapter IV), but no data are available on the switching of food sources by earthworms.
Organic matter may have been a limiting factor to the highest worm population. A population model describing the effects of food shortage on the population level of the worms would be needed to change the worm population according to the carrying capacity of the field.
The layer-boundary adjustment should be fine-tuned. The litter layer contained humus from cast after the mineral matter is transferred to the receiving layer. Inclusion of more soil layers could give a better simulation of the EARTHWORM SIMULATION MODELS / 125 changes in the soil profile. An organic matter gradient in
the soil could then be simulated.
This version of F-MIXER includes only one earthworm
strategy. Competition sub-routines are available and the model is set up to include more strategies. However, no data
could be found in the literature to calibrate competition
between earthworms. Data should be collected, using the
column technique, on the redistribution of cast in the soil
profile by other species. The results of the simulations
represented in Figure 12, should be validated in field plots
for which historical data on worm populations and soil
management are available. VI. GENERAL DISCUSSION
The egestion rate calculated from the column experiment is
5.2 times higher than that calculated from the litterbag technique (2.34 vs 0.45 g.g"1.day"1). Direct comparison of the two techniques for measuring egestion rates is difficult because the food source was not the same. In the litterbag technique, the food (clover hay) was collected from the field. This material had been in the field for several months and consisted of partly decomposed clover stems. The material used in the column experiment was grown in the greenhouse and consisted of young clover leaves. Young leaves are expected to decompose faster than the clover hay, and may contain a different microbial population. Large differences in egestion rates suggest that the young clover leaves are less palatable than the clover hay used in the litterbag technique. The palatability of the young clover leaves may be less, either because they contained undesirable substances such as phenols, or they contained only limited amounts of microorganisms. Hence the worms supplemented the clover leaves with large quantities of soil. The development of a food quality index based on the microbial activity and diversity should be helpful in future studies on earthworm feeding.
When the egestion of organic carbon was compared for the two
126 GENERAL DISCUSSION / 127 techniques, both techniques showed similar results: 37.1 ±
12.31 rng.g"1.day"1 in the litterbag technique , and 46.1 mg.g"1.day"1 in the transport experiment. In preliminary experiments, different kinds of foods were offered to
L. rubellus (5 °C, moist soil). The egestion rate ranged from 0.09 g.g^.day"1 for clover leaves, to 0.65 for soil.
The egested amount of carbon was 15.5 rng.g"'.day"1 in all cases (Appendix 3-B). When the egested amount of carbon was calculated for the 5 °C litterbag trial, the following values were found: 17.8 ± 6.4, 18.1 ± 5.3, 25.9 ± 5.9 and
12.7 ± 4.5 rng.g"1.day"1 for wet to dry soil environments
respectively. These values are not different from the one
found in the food selection trial. The findings from these three independent experiments lead to the conclusion that the amount of carbon egested by earthworms, compared to the
total egestion rate, is a superior parameter to measure the carbon needs and activity of earthworms.
The egestion rate of mineral soil plus organic matter can be
seen as the flow rate of a "carrier" through the gut of an earthworm. This flow is needed to satisfy the nutritonal
needs of the earthworm. Organic matter can be seen as a
superior food source, probably because of the large
population of microorganisms it contains. When the organic matter (litter) is not supplying enough nutrients, the worms GENERAL DISCUSSION / 128
ingest large quantities of soil, including humus, to make up any deficiencies. The total intake of organic matter is a constant factor, only dependent on soil temperature and soil moisture which both affect the metabolic activity of the
worms. Standards for temperature and moisture content in
ingestion or egestion experiments are needed to compare the
results for different species.
Only a small amount of organic matter is assimilated by
earthworms (e.g. Uvarov, 1982). It is well established that
some earthworm species feed on microorganisms (see section
II-A-2). The quality of food may well lay in the quantities
of microorganisms inhabiting (soil) organic matter. Tests
specifying the level of activity or quantities of
microorganisms may be used to specify the quality of worm
food.
Both the column experiment and the litterbag experiment were
conducted at constant temperatures. Results from these
experiments may not represent field situations. Diurnal and
seasonal temperature fluctuations may cause changes in worm
physiology, as was suggested by Reinecke and Kriel (1981).
At a fluctuating temperature of 20 °C, Eisenia foetida
produced fewer cocoons, but more hatchlings per cocoon than
at a constant temperature. More research is needed to GENERAL DISCUSSION / 129 clarify the exact effect of a fluctuating temperature on earthworm activity and physiology.
Although the egestion rates differed between both techniques, the litterbag and the column experiment gave similar results for the egestion rate of carbon. This means that both techniques were equally suitable for measuring the egestion rate of carbon. The litterbag technique does not require a large incubator and can be carried out in a small space. The column experiment has many advantages. It yields more cast per column to analyze and also provides the distribution of casts related to depth. The columns can be used both in the laboratory and in the field where excessive wetness is detrimental for the litterbag technique due to smearing of casts and soil by the earthworms.
Workers in Europe regard L. rubellus as a species with little influence on the soil structure (Bouche, personal communication, Edwards, personal communication). This may be based on the classification (epigeics), the low abundance in mature systems and on the assumption that the worm is a surface casting species. Small amounts of cast found on the surface, actually only 15 % of the total cast production, might therefore be seen as an indication of a low egestion rate. GENERAL DISCUSSION / 130
In Europe, L. rubellus is often found in association with other earthworms. Being a pioneer species, the worm may not be able to compete for food and space with other species once the habitat becomessuitable for K-strategists. Bouche
(1977) suggested that epigeics and anecics compete for food.
Abbot (1981) concluded from his competition experiments in the laboratory, that M. dubius did not do well in cultures with either E. foetida or AlI ol obophora trapezoi des . He suggested a toxic interaction between the species or that the availability of certain digestive enzymes in the superior species, would cause the decline.
In associations with other worms, L. rubellus may be forced to occupy the very top of the soil, not preferred by other species. The published information about the role and activity of L. rubellus may also lead to the hypothesis that this species developed different ecotypes: in Europe a surface dweller, and in North America a sub-surface dweller.
However, both in North America (this study) and in Europe, the worm was found in the lower layers of the soil (Persson and Lohm, 1977; Byzova, 1965). Byzova's observation that the respiration rates of L. rubellus were similar to those of mid-strata worms, would indicate that it is not an epigeic species. GENERAL DISCUSSION / 131
L. rubellus was active in the mineral soil-litter interface and created a burrow system. The worm also produced casts both in the litter layer (15 %) and in the mineral soil
(85 %). Therefore the hypothesis that the earthworm species only lives in the litter layer and only casts in this layer, is rejected. A new strategy class is hereby proposed to include L. rubellus: eurygeic species {evpv = wide), worms that live in the litter-soil interface and feed both on mineral soil and surface litter. Cast production is both in the litter layer and in the mineral soil. These worms may have morphological characteristics of both epigeic and endogeic worms, and are good soil mixers. This strategy is included in Figure 13. Bouche's classification (Bouche,
1977) is based on morphological characteristics, while the functional and spatial emphasis is implied. The eurygeic class is based on functional and spatial characteristics and may contain worms with different morphological characteristics. Bouche (1977) showed that several European lumbricids were not covered by the three main classes. Wood
(1974) distinguished two megascolecid worms from a mountain site in Australia, as topsoil species, with characteristics to fit the eurygeic class. These two species, Cryptodrilus fasligalus and Megascolex celmisiae fed on litter and on soil and occupied the top 10 cm of the mineral soil. Lavelle
(1979) grouped Dichogaster agi I i s and Millsonia I ami ol ana GENERAL DISCUSSION / 132
BC
SOIL AND ORGANIC MATTER TURN OVER
ORGAN ICS USED AS FOOD
Figure 13. Earthworm strategies as perceived from Bouche (1977) with a new class added. GENERAL DISCUSSION / 133 from Ivory Coast in an intermediate class between epigeic and endogeic. These non-lumbricid species would also fit in the eurygeic class, as would several topsoil species from
Lee's system (Lee, 1959, cited by Lee, 1985). Non-native
North American lumbricids that may be included in the eurygeic class are Aporrectodea caliginosa, Lumbricus festivus and L. castaneus. Adding the eurygeic class to
Bouche's system, would make it a strategy classification that is widely usable.
The first approximation of a simulation model to test the understanding of soil mixing by earthworms revealed many gaps in our knowledge on earthworm ecology. From the simulation of soil mixing and the integration of MIXER in
FORCYTE, it became apparent that several topics require further research. Earthworm feeding, including a "hunting routine", and the characterization of the food need attention. The question of intestinal flora versus the rapid development of microorganisms in the gut and faeces need to be resolved, and the question of the effects of fluctuating temperatures on earthworm behavior should be explored.
To run the simulation model for more than one species, basic data on the feeding and casting patterns are needed for all species (or groups of species) involved, as well as information on inter-species competition, establishment of GENERAL DISCUSSION / 134 quality determinations for earthworm food and population dynamics as related to different sites. VII. SUMMARY AND CONCLUSIONS
The objectives of the presented research were to describe the ecological strategy of Lumbricus rubellus
Hoffmeister, in relation to soil moisture, temperature and drought stress; to describe the transport of organic matter into the mineral soil; and to develop a model to simulate this transport.
The following approaches were used: a litterbag technique to study the effects of soil moisture and soil temperature on the egestion rate of L. rubellus and a column transport experiment in which 1ttC labelled clover material was offered as worm food, to study the food choice and the ability of the worm to transport soil and organic matter.
The litterbag technique was adapted to be used with earthworms; a soil-moisture-buffer system was added by incubating the litterbags in a basin with soil of a predetermined moisture content.
The column transport method was newly developed. Soil columns were equillibrated on a porous plate and earthworms were fed with radio-labelled clover shoots or roots. The egestion rate was calculated and the ratio of shoots to roots in the earthworm diet was determined.
This method appeared to be well suited to quantify
135 SUMMARY AND CONCLUSIONS / 136 egestion rates of earthworms.
Results from the litterbag experiment showed that both moisture and temperature affected the total egestion and ingestion rate of L. rubellus. The temperature effect was visible under 'wet' conditions, the moisture effect was pronounced under 'dry' conditions.
The earthworm reduced the intake of mineral soil when under drought stress to reduce water loss and ingested relatively more organic matter. The faecal water content was always above the liquid limit of the soil and the faecal carbon content was above that of mineral soil.
The body water content was related to the soil water potential. A maximum body water content was found at a soil water potential of -15 m of water.
Results of the column experiment showed that L. rubellus produced 15 % of its cast on the surface, 46 % in the
0-5 cm layer, 22 % in the 5-10 cm layer and 16 % in the
10-15 cm layer of the soil.
The worm preferentially ingested 78-82 % of the supplied organic matter as leaf litter and 18-22 % as root litter. The carbon content of the recovered cast was not significantly different in each of the soil layers; 1*C label originating from both surface litter and root SUMMARY AND CONCLUSIONS / 137
litter was recovered in cast throughout the profile.
These findings indicate that organic matter originating
from the litter layer was mixed into the profile by
L. rubellus.
8. The two techniques for measuring earthworm activity,
showed very different egestion rates for L. rubellus,
0.45 g.g-'.day"1 for the litterbag techinique and 2.34
g.g-1.day 1 for the column experiment. The egestion
rates of carbon, however, was similar (37.1 ± 12.31 vs
46.13 rng.g"1.day1, 10 °C). When the egestion of carbon
(5 °C) was compared with that found in a preliminary
food trial, both tests showed a similar egestion of
carbon (15.5 rng.g"1.day"1), similar to that found in the
litterbag technique (5 °C).
9. It was concluded that the ingestion of carbon reflects
the energy use of the earthworms and is a more suitable
parameter to measure earthworm activity than the total
egestion rate.
10. Based on the presented evidence, the earthworm
L. rubellus cannot be classified as an epigeic species.
A new ecological strategy class was introduced: eurygeic
worms, living in the litter-soil interface. Several
other non-native North American lumbricids and also some
Australian and African megascolecid species can SUMMARY AND CONCLUSIONS / 138
currently be included in this class.
11. A conceptual model for mixing of soil and organic matter
by earthworms was developed from the literature. This
model is a multi-species, non specific model, contrary
to the single-species, specific models presented in the
literature. Data from the present column experiment were
used to adapt the model as a sub-routine for FORCYTE, an
existing model for ecosystem management simulations.
Earthworms caused a decrease in the accumulation rate of
surface litter and and increase in the organic matter
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LUMBRICUS RUBELLUS HOFFMEISTER, 1843.
(Red Worm, Red Marsh Worm)
Diagnosi s
length 25 - 150 mm
diameter 4 - 6 mm
adult weight 52 -160 mg (dwt)
segments 95-120
tanylobic prostomium
first dorsal pore 7/8
clitellum xxvi, xxvii - xxxi, xxxii
tuberculata pubertatis on xxxviii - xxxxi
setae closely paired, aa:ab:bc:cd:dd = 5:1:5:5/6:19
dd=1/2 u and ab of x often on a pale genital tumescences
male pores inconspicuous, without glandular papillae on
xv
seminal vesicles, 3 pairs in 9, 11 and 12 + 13
spermathecae with short ducts opening in 9/10 and 10/11
colour: ruddy brown or red violet and iridescent
dorsally, pale yellow ventrally
body cylindrical and sometimes dorso-ventrally flattened
posteriorly
(Reynolds et al., 1974)
1 53 APPENDIX 2-A. DIAGRAM OF THE FUMIGATION SET-UP
Appendix 2-A. Diagram of fumigation set-up.
1 = clover plants; 2 = container with nutrient solution; 3 = plexiglass container; 4 = removable lid; 5 = seal; 6 = ventilator; 7 = membrane injection port; 8 = mixing vessel; 9 = heat absorbing water bath; 10 = light source.
1 54 APPENDIX 2-B. DIAGRAM OF THE SOIL COLUMN SET-UP
13
Appendix 2-B. Diagram of the soil column set-up.
1 = lid (500 ml container); 2 = seal; 3 = clover (shoots); 4 = clover (roots); 5 = soil; 6 = seal; 7 = porous plate (sand); 8 = ABS column and lid; 9 overflow unit; 10 = circulation pump; 11 = water recervoir; 12 = gas wash vessel; 13 = polypropylene tent; 14 = plexiglass container; 15 = mesh plug.
155 APPENDIX 2-C. SOIL MOISTURE AND SOIL TEMPERATURE ON WESTHAM
ISLAND
1
ID
Appendix 2-C, Figure A. Soil moisture and soil temperature on Westham Island, measured during 1983 and 1984. Soil temperature at 5 cm depth, soil moisture 0-5 cm: •-• ; 5-10 cm: o-o .
156 APPENDIX 2-D. THE POPULATION OF L. RUBELLUS ON WESTHAM
ISLAND.
Appendix 2-D, Figure A. The population of L. rubellus in two fields on Westham Island.
• • = Barley-clover after potatoes; o o = Clover-peas-clover; 1981 - Carter (unpubl.), 1982 - Carter and Timmenga (unpubl.), 1983 - Carter and Bandoni (unpubl.).
157 APPENDIX 2-E. RETENTION CURVE OF CRESCENT SERIES SOIL.
Appendix 2-E, Figure A. The water retention curve for the Crescent Series soil from Westham Island, British Columbia. • = Supplementary data from De Vries (Pers. Comm.)
158 APPENDIX 3-A. LENGTH OF LITTERBAG EXPERIMENTS.
The litterbag technique was used in several preliminary experiments. The length of the incubation was derived from the following table.
Appendix 3-A, Table A. The egestion rate of Lumbricus rubellus incubated at different periods (10° C., M = 0.39 kg.kg"1, n = 6)
Time (days) Egestion rate (±SD)
g.g 1.day
3.5 0.67 (0.314)
7.0 0.50 (0.134)
10.0 0.45 (0.091)
14.0 0.51 (0.146)
159 APPENDIX 3-B. FOOD CHOICES OF L. RUBELLUS
Using the litterbag technique, L. rubellus was fed on different food materials: partly decomposed clover leaves, partly decomposed clover leaves plus soil, partly decomposed clover hay plus soil, partly decomposed barley straw plus soil and soil. The soil was collected from the Westham
Island field, as described earlier. The worm showed remarkable differences in egestion rates (5 °C), the lowest rate was found for clover leaves, while soil reflected the highest rate. The total amount of carbon egested remained constant in all cases and there was a significant inverse linear correlation between the amount of carbon egested and the egestion rate (r = - 0.944, See Figure Appendix 3-B).
The calculated egestion of carbon was 15.5 mg.g"1 .day""1 for all food sources. The carbon content was measured as Leco carbon. Barley straw was not ingested by the worms, the particles were not shredded. However, it was noted that fungal colonies were removed from the straw and ingested.
160 / 161
Appendix 3-B, Figure A. The correlation between the egestion rate (g.g~1.day"1) of worms fed on different foods and the faeces carbon content (%) for L. rubellus (5 °C). APPENDIX 3-C. SIZE AND AGE OF L. RUBELLUS, AS RELATED TO THE
EGESTION RATE.
Mature clitellated adults and immature adults were incubated for 7 days at 10° C. and - 12.5 m of water. Immature worms showed a higher egestion rate than mature worms' (Figure A).
There was a significant negative correlation between weight and egestion rate when the population included both mature and immature worms (r = 0.737, Figure B).
162 / 163
o i i 1 0 - »0 - 20
WATER POTENTIAL (M OF WATER)
Appendix 3-C, Figure A. The egestion rate (g.g"1.day"1) of mature, clitellated and immature adults of L. rubellus, fed on clover leaves plus soil (10° C). / 164
o » • • 0 50 100 150 ZOO 25 0 WORM WEIGHT (MG)
Appendix 3-C, Figure B. The egestion rate (g.g-1.day"1) of L. rubellus as related to the worm weight (mg), for worms fed on clover leaves and soil (10 °C,) APPENDIX 4. THE EGESTION RATE OF A. CHLOROTICA.
The earthworm AlIolobophora chlorotica Savigny, 1826,. was an abundant species in the Westham Island clover field. A third less abundant species, was Eiseni el I a tetraedra
Savigny, 1826. A. chlorotica was tested in the litterbag technique on several occasions. In contrast to L. rubellus, this species burrowed through the soil clods in the litterbag and consumed only limited amounts of the offered organic matter. The egestion rate was three times as high as that of L. rubellus (1.09 (0.764) g.g-'.day"1 (SD), 6.04 % C in the cast, 15 °C) under similar conditions, and the carbon content of the faeces (2.33 % C in the cast, 15 °C) was slightly higher than that of the offered soil.
165 / 166
Appendix 4, Table A. The egestion rate of A. chlorotica under different environmental conditions.
Temp Season Moisture Specimens Egestion
°C m of w n (SD)
5 fall - 3 9 1.74 (0.404)
10 spring - 3 10 1.36 (0.603)
10 fall - 3 11 2.93 (1 . 160)
15 spring - 10 5 3.03 (0.764) APPENDIX 5. TURN-OVER OF SOIL AND ORGANIC MATTER CALCULATED
FROM THE LITTERBAG TECHNIQUE
The turnover of soil and organic matter by L. rubelllus was calculated using the method outlined by Lavelle (1975). For each monthly period, the average soil temperature (5 cm depth) and soil moisture content (0-5 cm) was calculated
(using data from Appendix 2-C) and the ingestion rate for organic matter and soil were interpolated using data from
Figures 3 and 4. The population biomass figures, collected by Carter (unpublished), and Carter and Timmenga
(unpublished) were used to calculate the total amount of soil and organic matter ingested by earthworms (population figures from Appendix 2-D).
A population of adult L. rubellus in an agricultural field and recovering from a major disturbance (harvesting of a potato crop followed by soil cultivation), ingested 1.9 tonnes.ha-1 organic matter and 14.6 tonnes.ha-1 mineral soil during a year. This estimate does not account for the exhaustion of organic matter and its effects on the worm population. The population figures used, reflect the recovery of a population after a major disturbance, the population may not have reached its limits. Total ingestion rate in each month was clearly influenced by soil temperatures, while drought effects were hardly visible.
167 / 168
Appendix 5, Figure A. The turn-over of soil (x) and organic matter (•) by a population of adult L. rubellus (August 1983 - September 1984; 1981-1982 population data were used,{o}.). / 169
Under Westham Island conditions the effect on ingestion rate caused by a drop in soil moisture content is not strong enough to significantly influence the effect of temperature.
Earthworms were active throughout the year; in wet winter months, when temperatures were only a few degrees above freezing, worms were active in the litter layer. During summer when soil temperatures reached 20° C, soil water tension became the limiting factor for earthworms and L. rubellus moved down into the profile; worms were found in cracks and old root channels at depth of 15 to 20 cm. Their burrows had accumulations of organic matter and were coated with mucus. In south coastal British Columbia, the soil temperature rarely exeeds the optimum temperature range (15
- 18 °C) of this species. APPENDIX 6. DETAILED DESCRIPTION OF F-MIXER.
FORCYTE VERSION 11:11
SOILSDATA
Input data not site specific. Section 1.5:
specify soil layers (n, layer 1 is Litterlayer) specify availability of earthworms (yes/no) specify humus type from cast ingestion pattern of worm (% total ingestion, weight basis per layer) egestion pattern of worm (% total egestion, weight basis per layer) specify youngest age of litter used by worms
Input data site specific. Section 2.10:
mass of mineral soil in layers (no stones) mass of humus in layers
maximum worm biomass on the site (kg/ha) population recovery (time steps or population dynamics) ingestion rate of organic matter (kg/kg.time step) to sustain population maximum throughput.of cast (kg/kg.time step) assimilation rate for humus (% weight loss) assimilation rate for litter (% weight loss)
Data input for simulation of column experiment:
biomass of worms (kg/ha) time steps for duration of experiment (nn) population dynamics switch (yes/no) *to allow to hold population constant or to fluctuate population with available organic matter.
added litter to surface (kg/ha) decomposition type of this litter added fine root biomass to soil (kg/ha) decomposition type of fine roots distribution of root litter in specified layers
FORSOIL SIMULATION OF COLUMN EXPERIMENT
Normalisation of distributions (ingestion, egestion, root litter distribution foliage litter on top of soil (layer 1)
No worms, (1.5) sub-program is deleted from program run
Initialize various output parameters (cast per layer, decomp. per layer, humus per layer, organic concentration
170 per layer
Initialize nutrient parameters (content in layer:, in humus, in litter; from 2.5, 2.10)
Initialize tabular output headings: time, wormmass, littermass ingested, humus mass Ingested, soil mass Ingested, cast mass egested for n layers (current)
litter mass for n layers (total distribution) humus mass for n layers (total distribution)
soil mass for n layers (current timestep only) % OM for n layers
RUNNING OF F-MIXER (Loop over time)
Zero values that describe the sums of added humus, added litter, net release nutrients
Redistribute soil and organic matter to re-align soil layers •Initial amount of mineral soil In each layer 1s saved (from 2.10). The mixing by worms 1n the previous time step has upset the layer content. To correct the layer content the following calculation Is done for each time step exept the first one. To start with bottom layer, compare available mineral soil with the Initial, a net difference 1s transported to/from the layer above m order to regain the initial soil mass. Humus 1s transported with the mineral soil according to the concentration of the layer where the soil comes from.
Decompose existing litter (rates from SOILDATA 2.8) •Method of decomposition: second last age class compared with last in array, nutrients are released according to change in mass and nutrient content (litter 2.7; humus -2.5, pattern of change 1.4) net release of each nutrient is summed
Add litter to each soil layer (2.10)
Calculate expected amount OM Ingested •This amount is calculated from the worm biomass and the need of OM to sustain the population.
Allocate ingestion per layer
Allocate potential OM ingested per layer (soil + humus + litter) •The potential OM ingested is calculated from the humus and litter content of the soil layers. It 1s the summation of the proportion of OM for each layer. / 172
Soil 1s Ingested, rocks are exluded from the total mass of soil. Unused decomposables included in the soil, but separately specified, are not ingested.
Compare potential with expected amount of ingested OM
Worms ingest the potential amount of mix
Apply assimilation rates: ingested material is reduced
Redistribute the cast into the soil layers according to given proportions (1.5) Soil humus decomposition: nutrient release
Transfer last decomposition class of litter to humus
Transfer cast to humus, humus and soil are distributed as specified for each layer, all decomposition types go to specified humus class, release of nutrients
Calculate OM concentration for each soil layer
Calculate cast for each layer
Worm population switch •Population 1s constant, each time step, the same amount of biomass 1s added to the column, or, when switch is in use, the population will Increase or decrease depending on the amount OM available. The maximum population is taken into account.
Create output 1ine Publications
Timmenga, H.J., 1983 Effects of soil moisture, soil temperature and food quality on the turn-over rate of organic and mineral matter by the earthworm Lumbricus rube!lus in a clover system. AIC/CSSS Meeting, Truro, Nova Scotia, 1983. Abstract published in Proceedings. Timmenga, H.J., and D. Pederson, 1984. Earthworm population densities in a drained and an undrained field of the Boundary Bay Water Management Research Project. Internal Report for the British Columbia Ministry of Agriculture and Fisheries, Cloverdale, B.C. 7 pp. Timmenga, H.J., 1984. The possible effects of artificial acid rain on soils, crops and soil biota. Year Report 1982-83, Faculty of Agriculture, UBC, Vancouver. 20-21. Timmenga, H.J., 1984. The water relations of the earthworm Lumbricus rubellus io a clay loam soil. CSSS Meeting, Banfff, Alberta, 1984. Abstract published in Proceedings. Carter, A., T.F. Guthrie, E.A. Kenney, H.J. Timmenga, 1984. Heavy metals in earthworms in non-contaminated
and contaminated soils from;near Vancouver. In: Earthworm Ecology, J.E. Satchell, editor. Chapman and
Hall, London. 267-274. fe Schreier, H. and H.J. Timmenga., 1986. Earthworm response to asbestos rich serpentinitic sediments. Soil Biol. Biochem. 18: 85-89. Timmenga, H.J., 1986. The fertilizer and chemical products market of the Nursery and Greenhouse Industries in the south Coastal Region of British Columbia. Consultants Report for Coast Agri Fertilizer Ltd., Abbotsford, B.C. 14 pp. Timmenga, H.J., 198/. Soil degradation in British Columbia. Butter fat, Oairyland Foods, Burnaby. (in press). Timmenga, H.J., 1987. Soil conservation in British Columbia. Butter fat, Dairyland Foods, Burnaby, (in press).