A Survey of Tropical

Ea.rthworms: Taxonomy,
Biogeography and
Environmental Plasticity
3
Carlos Fragoso\ Jean Kanyonyo2, Ana Moreno ,
4 5
Bikram K. Senapati , Eric Blanchart and Carlos
6
Rodriguez
l Departamento Bi%gfa de Sue/os, Instituto de Ec%gfa,

Xa/apa, Mexico; 2 Université du Rwanda, Butare, Rwanda;

3 Un iversidad Comp/utense, Madrid, Spain; 4Schoo/ of Life

Sciences, Samba/pur University, Samba/pur, India; 5 Laboratoire

B.O.s. T., IRD, Fort-de-France, Martinique; 6Universidad de /a
Habana, La Habana, Cuba

Summary

A worldwide survey of earthworms in the humid tropics revealed that 51

exotics and 151 native species are commonly found in tropical
agroecosystems. On the basis of frequency records and climatic and edaphic
ranges, 21 exotics and 27 native species have been selected as possible candi-
dates for manipulation. A multivariate analysis separated these species into
four groups: (i) native species with wide edaphic and medium climatic toler-
ances; (ii) exotic species with wide climatic and edaphic tolerances; (iii) native
and exotic species with narrow edaphic tolerances but more resistant to
climatic variations; and (iv) native species with limited tolerance for climatic
and edaphic variations.
Regarding management, species of group (ii) seem to be the most adapt-
able. both at regional and locallevels (multipurpose species); group (i) can be
managed for specific climatic conditions whereas group (iii) should be
managed in specific soil environments. Species of group (iv) may only be
managed at a very local scale.

©CAB International 1999. Earthworm Management in Tropical Agroecosystems

(eds P. Lavelle, L. Brussaard and P. Hendrix)
2 C. Fragoso et al.

Introduction

Earthworms are confmed to the soil and, for the majority of tropical farmers
and agronomists, their diversity, activities and eiTects on soils are totally
unknown. Even in the field of tropical soil science, the situation is not very dif-
ferent. For example, just a few years ago, there was little concern about earth-
worm diversity and the possible role of this diversity in the fertility of
agroecosystems. During the last 10 years, however, there has been an increas-
ing interest in diversity mainly due to the biodiversity crisis, which could be
defined as the dramatic loss of species, habitats and ecological interactions
(Wilson, 1985; Wilson and Peter, 1988; McNelly et al., 1990). Although the
most diverse tropical biota are insects that spend part of their life cycles in the
sail, this environment has been, from a biodiversity viewpoint, one orthe least
studied.
Earthworms are not very diverse, and our current estimations of the
number of existing species are far from complete. The most recent account of
earthworm diversity (Reynolds, 1994) comprises 3627 earthworm species
described worldwide, with an average annual addition of 68 species. The
overall richness is expected to be at least twice this value, with the majority of
still unknown species living in the tropics. For most species, the original
description is the only information available, and nothing is known about their
distribution, ecology, demography, physiology and resistance to disturbance.
For example, on the basis of the number of native species found in two moder-
ately well sampled regions, the state of Veracruz, Mexico, 33 species (Fragoso,
in press), and Puerto Rico, 18 species (Borges, 1988; Borges and Moreno,
1989, 1990a,b, 1991, 1992), it is possible to predict the possible number of
native species to be found in six scarcely sampled countries: three Central
American continental countries (Honduras, Nicaragua and Guatemala) and
three larger Caribbean islands (Cuba, Hispaniola and Jamaica). In the first
group, nearly 50 species per country should be found in the future, whereas in
the second group the number of species expected to be discovered is approx-
imately ten (Jamaica), 130 (Hispaniola) and 200 (Cuba). This means that if
sampling in these two regions is made with an eiTort similar to that in Veracruz
and Puerto Rico, we should expect to find nearly 500 new native species in the
future. Similar conclusions have been reached for Tasmania and Australia,
where 150 and 600 species, respectively, are expected to be found once
inventories are completed (Kingston and Dyne, 1995).
This chapter is the result of a 6-year project focused on characterizing the
identity of earthworms in natural and managed ecosystems of the tropics (out-
lined in Fragoso et al., 1995). The main objective was to select a group ofearth-
worm species with potential for management in tropical agroecosystems,
according to the following criteria: (i) a wide distribution; (ii) with adaptations
to a wide range of environmental and edaphic conditions; and (Hi) resistance to
disturbances induced by agriculture.
 A Survey of Tropical Earthworms 3

Storage and Analysis of Data

The survey was conducted in selected regions of the tropics, and included field
sampling and literature data. Most field data were obtained from the experi-
mental sites related to this project (the MACROFAUNA network, see Chapters
4 and 5). Although it was not the principal objective, this survey allowed the
discovery and description of approximately 50 new species.

EWDBASE: a database of tropical earthworms

All the information was stored in a database (EWDBASE) that includes infor-
mation on the taxonomy and distribution of earthworm species, earthworm
and other macroinvertebrate communities, climate of localities, edaphic and
land-use variables, and socioeconomic aspects of agricultural lands where
available.
Inputs to EWDBASE (climatic, edaphic and species distribution data) were
taken from the following published literature: Mexico, Central America and
the Caribbean islands (Eisen, 1895, 1896, 1900; Michaelsen, 1900, 1908,
1911, 1912, 1923, 1935, 1936; Cognetti, 1904a,b, 1905, 1906, 1907,
1908; Pickford, 1938; Gates, 1954, 1962a,b, 1970a,b, 1971, 1972, 1973,
1977a,b, 1979, 1982; Graff, 1957; Righi, 1972; Righi and Fraile, 1987; Sims,
1987; Borges, 1988, 1994; Borges and Moreno, 1989, 1990a,b, 1991, 1992;
Fraile. 1989; James, 1990, 1991, 1993; Csuzdi and Zicsi, 1991; Zicsi and
Csuzdi, 1991; Fragoso, 1993, in press; Rodrfguez, 1993; Fragoso and Rojas,
1994; Reynolds and Guerra, 1994; Reynolds and Righi, 1994; Fragoso et al.,
1995; Reynolds et al., 1995; Rodrfguez and Fragoso, 1995), Bolivia (Rombke
and Hanagarth, 1994), Ivory Coast (Omodeo, 1958; Lavelle, 1978, 1983;
Tondoh. 1994), Congo (Zicsi and Csuzdi, 1986), Ghana (Sims, 1965), Gambia
(Sims, 1967), Peru (Yurimaguas; Lavelle and Pashanasi, 1988) and several
regions from India (Senapati, 1980; Chaudry and Mitra, 1983; Julka, 1986,
1988; Julka and Paliwal, 1986; Julka and Senapati, 1987; Bhadauria and
Ramakrishnan, 1989; Julka et al., 1989; Bano and Kale, 1991; Blanchart and
Julka, 1997). EWDBASE was also fed with data obtained from field sampling
carried out in Mexico, Panama, Colombia, Ivory Coast, India, Martinique,
Guadaloupe, Rwanda, Peru, Congo and Cuba by members of the macrofauna
network.
EWDBASE included data relating to 457 species, 745 localities and 836
sites from 28 countries. Distribution and environmental plasticity were ana-
lysed by relating species distribution to climate (1310 records), soils (818
records) and types ofland use (1755 records).
4 C. Fragoso et al.

Data analysis

Data were analysed at three geographic levels, Le. local, regional and world-
wide. At the locallevel, we intended to characterize the persistence of native
earthworm species in difIerent land-use systems (e.g. conversion of tropical
deciduous forests to maize or pastures in Panuco, Mexico; maize plantations in
native savannas of Lamto, Ivory Coast or the eastern llanos of Colombia; tea
plantations in cloud forests of India, etc.). At the regionallevel, the analysis
was extended to geographic areas such as southern Mexico, northern Rwanda
or the Baoule region around Lamto (Ivory Coast), with the aim of identifying
widespread native species. The worldwide analysis evaluated the distribution
of exotic species in difIerent natural and managed tropical ecosystems. The
integration ofthese data in a global analysis produced three main outputs: (i) a
list of tropical species of worldwide distribution that can be manipulated in any
agroecosystem; (ii) regional lists of species by countries and/or kinds of
agroecosystems; and (iii) an evaluation of the environmental and edaphic
plasticity of these selected species.
Earthworm species ofEWDBASE were classified along three difIerent axes:
1. Biogeography, to divide species depending on this origin into natives and
exotics. Native earthworms are those species that evolved in the site or region
under study. Exotic species are earthworms that did not originate in the site
under study and that were, generally, introduced by human activities; these
species have also been called peregrine (Lee, 1987) and anthropochorous
(Gates, 1970c).
2. Distribution among land-use systems, to separate species on the basis of
their capabilities to adapt to natural (e.g. primary forests or savannas) or
managed (e.g. annual crops or pastures) systems.
3. Ecological plasticity, to rank earthworms according to their ecological tol-
erance to edaphic and environmental variables from stenoecic (narrow range)
to euryoecic (wide range) species.
These three axes were combined with the three geographic scales ofanaly-
sis (local,·regional and global) in order to propose the most appropiate earth-
worm species for manipulation in a given region and/or country in a specific
agricultural situation.

Earthworm Species of Tropical Agroecosystems

The exotic earthworms of the tropics

Since the early studies of Eisen (1900) and Michaelsen (1903, 1935), it has
been observed that peregrine worms were very common in tropical disturbed
ecosystems. In a paper that analysed the distribution and dispersal of this
 A Survey of Tropical Earthworms 5

group of species, Lee (1987) stated that these species '... more than any
others, ... are important in maintaining soil fertility in agricultural and pasto-
raI lands.' Although the author did nat present the complete list of species, he
mentioned that peregrine species comprise nearly 100 species (approx. 3% of
aH earthworms). Peregrine earthworms become exotics when the geographic
area of occurrence does not correspond to the original area of distribution.
The number of records of tropical exotic species is enormous, and their dis-
tribution should be analysed using the three scales mentioned above (world-
wide, regional and local), because sorne species with wide distributions may be
restricted to one kind of land-use system or have narrow climatic and edaphic
niches that are not represented in a given country or continent.
From EWDBA8E and a literature review (Gates, 1972,1982; Lee, 1987;
Mele et al., 1995), we identified 51 exotic species commonly distributed across
tropical countries (Table 1.1). Fifteen were temperate Lumbricidae of Euro-
pean origin, restricted to high altitude mountain localities. Their frequent
occurrence in natural temperate forests suggests that these species may have
replaced natives, as has been observed by Fragoso (in press) in the temperate
forests of Veracruz, Mexico. The absence of this group ofexotics in low altitude
tropical agroecosystems (from EWDBA8E queries) eliminates their potential
for manipulation and, therefore, this group of species will no longer be consid-
ered in this chapter.
From Table 1.1, we selected a group of 20 species distributed worldwide,
which are mainly from localities below 1000 m. This group is presented in
Table 1.2, ranked according to their frequencies in agroecosystems; Table 1.3
shows, for the above group of species, the ranges of environmental (precipita-
tion and temperature) and edaphic (pH, organic matter, nitrogen, sand and
clay) situations in which they occur. From the data in Tables 1.2 and 1.3, it is
possible to make a preliminary separation of another group of species adapted
to difIerent managed agroecosystems and with wide ranges of environmental
and/or edaphic plasticity. These species include Pontoscolex corethrurus,
Polypheretima elongata, Dichogaster bolaui, OcnerodriIus occidentalis, Amynthas
graciIis, A. corticis, Dichogaster affinis and D. saliens, and aH of them are tolerant
to very low soil concentrations ofnutrients, organic matter and nitrogen.

The widespread native earthworms of the tropics

The majority ofnative species are not very tolerant and are restricted mainly to
natural environments. Of the 404 native species stored in EWDBA8E, 274
species (67%) were restricted to a single locality, whereas 207 (51 %) were
found exclusively in natural environments. On the other hand, nearly 40% of
native species ofEWDBA8E were found inhabiting at least one of five types of
agricultural land-use systems: pastures, crops, tree plantations, organic
wastes and faHows (Table 1.4). Only a smaH proportion of these native species,
Continued p.16
Table 1.1. The exotic earthworms of the tropics. Continental, country and altitudinal distribution.

Distribution
Altitude (m)
Species Family Origin Continents Countries (average)

All%bophora ch/orotica Lumbricidae Europe 3 34 3000

Amynthas corticis Megascolecidae Asia 5 40 0-2500 (1243)
Amynthas gracilis Megascolecidae Asia 5 31 0-2000 (962)
Amynthas morrisi Megascolecidae Asia 4 23 610
Amynthas rodericensis Megascolecidae Asia 3 26 0-1200 (420)
Aporrectodea ca/iginosa Lumbricidae Europe 4 15 1150-3850 (3168)
Aporrectodea /onga Lumbricidae Europe 5 27 2240-2400
n
Aporrectodea rosea Lumbricidae Europe 5 52 500-4650 (2972) ."
Aporrectodea trapezoides Lumbricidae Europe 5 19 1200-3300 (2650) iiJ
Aporrectodea turgida Lumbricidae Europe 5 20 1300-3400 (2570) ~
ln
c
Bimastos parvus Lumbricidae N. America 5 32 12-1500 (756) ~
Bimastos tumidus Lumbricidae N. America 1 1 1000-1270 (1135) li>

Oendrobaena octaedra Lumbricidae Europe 4 32 1200-4650 (2423)

Oendrodri/us rubidus Lumbricidae Europe 5 46 950-4650 (2442)
Oiachaeta thomasi Glossoscolecidae S. America 1 2 Sea level
Oichogaster affinis Dichogastrini* W. Africa 4 24 0-1400 (391)
Oichogaster annae Dichogastrini* W. Africa 2 5 60-1940 (1438)
Oichogaster bo/aui Dichogastrini* W. Africa 5 43 0-1360 (259)
Oichogaster gracilis Dichogastrini* W. Africa 2 2 Under 500
Oichogaster modigliani Dichogastrini* W. Africa 4 20 0-1100 (339)
Oichogaster saliens Dichogastrini* W. Africa 4 17 0-1100 (307)
Orawida barwelli Moni 1igastridae India 2 11 0-1 000 (347)
Eisenia fetida Lumbricidae Europe 5 45 1300-1500 (1394)
Eiseniella tetraedra Lumbricidae Europe 5 45 1300-3820 (3109)
Eudrilus eugeniae Eudrilidae W. Africa 4 31 0-60 (15)
Eukerria kukenthali Ocnerodri 1idae S. America 2 8 n.d
Eukerria mcdonaldi Ocnerodrilidae S America 1 1 300
Eukerria peguana Ocnerodrilidae S. America 1 1 n.d.
Eukerria saltensis Ocnerodrilidae S. America 4 10 550-3875 (1911)
Eukerria zona lis Ocnerodrilidae S. America 1 1 300
Cordiodrilus peguanus Ocnerodri 1idae C. Africa 4 7 n.d.
Hyperiodrilus africanus Eudrilidae W. Africa 1 6 n.d.
Lumbricus rubellus Lumbricidae Europe 5 34 1500-3750 (2739)
).
Lumbricus castaneus Lumbricidae Europe 3 23 n.d. v.,
Lumbricus terrestris Lumbricidae Europe 5 36 n.d. ...,e:
Metapheretima taprobanae Megascolecidae Asia 4 7 10-40 (30) ~
'<:
Metaphire californica Megascolecidae Asia 5 21 0-2000 (982) 0
......
Metaphire houlleti Megascolecidae Asia 5 20 10-853 (408) :;i
Metaphire posthuma Megascolecidae Asia 2 12 12-22 (17) .g
r;'
Microscolex dubius Acanthodrilinae* S. America 5 16 n.d. ~
Microscolex phosphoreus Acanthodrilinae* S. America 5 28 1500-3600 (1506) [G1
Nematogenia panamaensis Ocnerodrilidae C. America 3 12 n.d. g.
Ocnerodrilus occidentalis Ocnerodrilidae C. America 5 22 0-1520 (470) ~
Octolasion cyaneum Lumbricidae Europe 5 30 1050-2430 (1576) ~
Octolasion tyrtaeum Lumbricidae Europe 5 35 1180-4654 (231 3) '"
Periscolex brachycystis G lossoscolecidae C. America 1 4 0-500 (192)
Peryonix excavatus Megascolecidae Asia 4 19 300-1050 (1077)
Pheretima bicincta Megascolecidae Asia 3 12 30-1100 (577)
Polypheretima elongata Megascolecidae Asia 4 27 0-1300 (185)
Polypheretima taprobanae Megascolecidae Asia 4 7 1360
Pontoscolex coreth ru rus G lossoscolecidae S. America 4 56 0-2000 (463)

*Tribe or subfamily of Megascolecidae; n.d. = not determined.

Table 1.2. Distribution of common exotic earthworms in different tropical land-use systems. No. of records from Mexico, Central
America, the Caribbean, Colombia, Rwanda, Congo, Ivory Coast and India.

Natural Tree
Species ecosystems Crops Pastures plantations Fallows Organic wastes

Pontoscolex corethrurus 94 31 44 41 6 4
Polypheretima elongata 30 10 39 19 4 5
Dichogaster bolaui 11 7 15 11 3 5
Ocnerodrilus occidentalis 3 6 15 7 2 1
Amynthas gracilis 7 4 6 9 2 2
Amynthas corticis 22 6 7 4 2 2
Hyperiodrilus africanus 2 4 8 5 1 2 !l
Dichogaster affinis 9 5 5 7 1 0 ..."
til
Dichogaster saliens 5 1 9 4 1 0
~
Drawida barwelli 3 1 9 3 0 0 <Il
0
Eudrilus,eugeniae 2 0 3 3 0 4 ~
Dichogaster annae 0 2 2 4 0 1 ~

Amynthas rodericensis 24 1 5 3 0 0
Peryonix excavatus 1 0 1 1 0 5
Metaphire californica 0 0 4 0 0 1
Dichogaster modigliani 1 0 4 1 0 0
Metaphire houlleti 0 0 4 0 0 0
Metapheretima taprobanae 2 0 2 1 0 0
Periscolex brachycystis 6 1 2 1 0 0
Pheretima bicincta 5 0 0 1 a a
Metaphire posthuma 1 a a 1 a a
Table 1.3. Range of environmental conditions tolerated by the most common exotic species.

Ca Mg
T Rainfall aM N (mEq (mEq S C
Species (oC) (mm) pH (%) (%(x 0.1)) 100 g-l) 100 g-l) (%) (%)

Pontoscolex corethrurus 14-28 268-5000 3.8-8.2 0.9-12.6 0.1-9 0.8-16.5 0.1-11.2 3-91 6-87
Polypheretima elongata 21-30 800-4000 5-7.8 1.8-7.6 0.8-3.8 4.4-53 1-2.7 5-93 4-54
Dichogaster bolaui 18-30 800-4725 5-8.2 1-10.2 0.2-8.8 1.7-44 0.06-9 5-93 4-53
Ocnerodrilus occidentalis 16-30 146-4725 5.6-8.9 0.9-7.8 0.7-8.9 0.8-53 0.06-4.5 18-98 2-74 ~
V)
Amynthas gracilis 15-26 670-3500 4.8-8.9 1.7-14.4 0.7-5.9 1.3-3.4 0.7-.46 11-61 9-53 c::
Amynthas corticis 13-26 865-4521 3.9-7.5 2-12.6 2-4.2 1.9-5.8 1.5-3.5 36-61 17-33 ~
'<::
Dichogaster affinis 17-28 440-2240 4.5-8.2 1-13.7 0.7-8.8 0.82-53 0.06-4.9 9-98 2-74
Dichogaster saliens 22-28 916-4725 5-8.9 0.6-6.2 0.2-8.9 0.9-12.5 0.06-4.5 18-91 6-47 ....
0
::;l
Drawida barwelli 21-26 1500-4000 5-7.9 3.6-5.4 2-2.5 3.5-5.8 1.1-3.5 3-42 24-87 0
~
Eudrilus eugeniae 25-28 1352-1880 n.d. n.d. n.d. n.d. n.d. n.d. n.d.
Dichogaster annae 28 1880 3.7-6.3 1.6-4.9 1-2.6 n.d. n.d. 32-85 11-54
[
Amynthas rodericensis 20-26 1200-5000 4.7-8 n.d. n.d. n.d. n.d. n.d. n.d. !i\1
::l.
:l""
Peryonix excavatus 15-24 865-2173 7.1-7.5 3 n.d. n.d. n.d. 50 33
Metaphire californica 21 2631 5.2-5.6 4.3-5.4 2.2-2.5 3.5-5.8 1.5-3.5 36-42 24-28 ~
Metaphire houlleti 22-26 1314-1996 6.8 2 n.d. n.d. n.d. n.d. n.d. 3
III

Metapheretima taprobanae 26 1450-2000 6.4-8 n.d. n.d. n.d. n.d. n.d. n.d.
Dichogaster modigliani 25 1396 n.d. n.d. n.d. n.d. n.d. n.d. n.d.
Periscolex brachycystis 24-28 1880-4725 5-6.5 2.2-7.6 1.1-4.2 4.1-44 1.1-3.6 5-62 9-50
Pheretima bicincta 21-26 2500-3500 n.d. n.d. n.d. n.d. n.d. n.d. n.d.
Metaphire posthuma 24 916-1079 8.1 1.2 1 6.6 0.86 46 18

T = temperature, aM = organic matter, N = nitrogen, Ca = calcium, Mg = magnesium, S = sand, C = clay; ail values from the upper 10 cm
of soil.
<.0
10 C. Fragoso et al.

Table 1.4. Native earthworm species of tropical agroecosystems.

Species C P T F W
Belize
Diplotrema jenniferae
Bolivia
Andiorrhinus bolivianus
Enantiodrilus borelli
Eukerria asuncionis
Eukerria eiseniana
Eukerria garmani
Eukerria tuberculatus
Goiascolex vanzolinii
Colombia
Andiodrilus yoparensis 1
Andiorrhinus sp.nov1 1
Glossodrilus sikuani 1 1
Glossodrilus spl 1 2 2 3
Martiodrilus agricola 1 2
Martiodrilus carimaguensis 1
Martiodrilus savanicola 1 1
Martiodrilus sp1 1 3
Thamnodrilus sp1 2
Congo
Dichogaster graffi
Gordiodrilus sp1
Nematogenia lacuum
Costa Rica
Glossodrilus dorasque
Glossodrilus nemoralis 4
Glossodrilus orosi 1
Cuba
Diplotrema ulrici 1
Onychochaeta elegans 1 4 4
Onychochaeta windlei 2 2 3
Pontoscolex cynthiae 1 3
Zapatadrilus morenoae 1
Zapatadrilus siboney
Zapatadrilus taina
El Salvador
Eutrigaster sporadonephra
Guadaloupe
Pontoscolex spiralis 2
 A Survey of Tropical Earthworms 11

Table 1.4. Continued.

Species C P T F W
India
Curgiona narayani 3
Drawida ampullacea 1 3 1 2
Orawida assamensis 1
Drawida calebi 1 1 2
Orawida fakira 1
Orawida ferina 2
Orawida ghatensis
Orawida japonica 1
Orawida kanarensis 1
Orawida lennora 1
Orawida modesta 1
Drawida nepalensis 1 2
Drawida paradoxa 1 10
Orawida pellucida 2
Orawida spl 1
Orawida sp2 1
Orawida scandens 1
Orawida sp3 4
Orawida sulcata
Orawida thurstoni 4
Drawida willsi 1 3 1
Eutyphoeus festivus 2
Eutyphoeus incommodus 2 3
Eutyphoeus orientalis 1
Eutyphoeus spl
Eutyphoeus waltoni
Gen.nov1 sp.nov1 8 1
Gen.novl sp.nov2 2
Gen.nov2 sp.novl 1
Gen.nov3 sp.novl 3
Clyphidrilus tuberosus 2
Clyphidrilus annandalei 2
Hoplochaetella kempi 1
H. sanvordemensis
Hoplochaetella suctoria
Hoplochaetella spl 1
Hoplochaetella sp2 2
Karmiella kamatakensis 6 1
Karmiella spl 1
Konkadrilus sp1 6 1 1
Konkadrilus sp2 8 2
Konkadrilus tirthahalliensis 6
Lampito mauritii 3 2 5
Lennogaster chittagongensis 1

Continued
12 C. Fragoso et al.

Table 1.4. Continued.

Species C P T F W
Lennogaster pusillus 3 3
Lennogaster sp1 1
Lennosco/ex sp1 1
Lennogaster dashi 2
Mallehulla indica 1
Megasco/ex fe/icisetae 1
Megasco/ex sp1 3
Megasco/ex insignis 1 1 1
Megasco/ex konkanensis 2 2 3
Megasco/ex /awsoni 2
Nellosco/ex strigosus
Notosco/ex sp1
Octochaetona beatrix
Octochaetona rosea
Octochaetona surensis
Pellogaster benga/ensis
Perionyx sp1
P/utellus tumidus
Ramiella bishambari
Tonosco/ex horaii 2
Travoscolides duodecimalis
Wahosco/ex sp1 4
Ivory Coast
Agastrodrilus opisthogynus 1
Chuniodrilus palustris 10 1 1 3
Chuniodrilus zielae 10 1 1 3
Dichogaster agilis 9 1 2 2
Millsonia anoma/a 9 1 1 3
Millsonia /amtoiana 1 1 1
Millsonia sch/egeli 2
Jamaica
Eutrigaster grandis
Martinique
Pontosco/ex cuasi 1
Pontoscolex spiralis 2 2
Mexico
Ba/anteodrilus pearsei 4 10 1 2 2
Dip/ocardia eiseni 1
Dip/ocardia sp.nov1 6
Dip/ocardia sp. 1
Dip/ocardia sp.nov2 3 6
Dip/otrema sp.nov1 1
Diplotrema murchiei 1 11 3
 A Survey of Tropical Earthworms 13

Table 1.4. Con tin ued.

5pecies C P T F W
Oiplotrema papillata 4
Gen.nov4 sp.novl 3
Gen.novS sp.novl 1
Larsonidrilus microscolecinus 2
Larsonidrilus orbiculatus 3
Lavellodrilus maya 3
Lavellodrilus parvus 5 5 1 1
Lavellodrilus riparius 1
Mayadrilus rombki
Phoenicodrilus sp.novl 1
Phoenicodrilus taste 1 16 2
Protozapotecia australis 1 6 1 1
Ramiellona sp.novl 1
Ramiellona sp.nov2
Ramiellona sp.nov3
Ramiellona sp.nov4
Ramiellona sp.novS
Ramiellona sp.nov6
Ramiellona sp.nov7 1
Ramiellona strigosa 1 2
Ramiellona wilsoni 1
Zapatadrilus sp.nov1 3 3 9 3
Zapotecia amecameca 1
Zapotecia nova 4 3
Zapotecia sp1 3 1
Peru
Oiachaeta xepe 1 2 1
Rhinodrilus lavellei 1 1
Rhinodrilus pashanasi 1 1 1
Rwanda
Oichogaster itoliensis 2 1 1
Oichogaster sp1 1 1 2
Eminoscolex lavellei 3 1 5
Gordiodrilus sp1 4 1 15
Stuhlmannia variabilis 1 2

No. of records from EWDBA5E. C=crops, P=pastures, T=tree plantations,

F=fallows,W=organic wastes.
Table 1.5. Environmental tolerance ranges (c1imatic and edaphic) of selected tropical native earthworms (data from EWDBASE).
.l>-

Ca Mg
T Rainfall aM N (mEq (mEq 5 C
Species (OC) (mm) pH (%) (% (x 0.1)) 100 g-l) 100 g-l) (%) (%)

Cuba
a. e/egans 28 1880 n.d. 7.6 n.d. 44 9 5 50
India
D. ampullacea 22 5000 4.6-5.8 4.3-11 0.17-0.48 2.5-14 1-3.7 15-43 18-53
D. paradoxa 22 5000 4.4-5.1 3.6-9.3 0.19-0.33. 2.4 0.93 23 40
D. wil/sii 30-31 1150-2363 5.9-6.8 0.9-2.4 0.08-0.38 n.d. n.d. 83-95 2-7
E. incommodus 16-30 1014-1600 5.9-6.8 1-3 n.d. n.d. n.d. n.d. n.d. n
D. nepa/ensis 16-26 1014-1600 6.7-6.8 1-2 n.d. n.d. n.d. n.d. n.d. ~
tU
K. karnatakensis 22 5000 4.7-5.5 4.2-7.5 0.17-0.33 5.04 1.71 28 18-40
L. mauritii 24-31 865-2166 6-6.7 1-3.2 0.08-0.19 n.d. n.d. 83-91 4-7 ~
li>
0
L. pusillus 16-30 1014-1700 5.9-6.8 1-5 n.d. n.d. n.d. 47 34 !S
a. beatrix 16-24 865-1314 6.8-7.1 2 n.d. n.d. n.d. n.d. n.d. ~
K. spl 22 5000 4.4-5.8 4.2-11 0.17-0.48 14.8 3.74 n.d. 18-53
K. sp2 22 5000 4.4-5.8 3.6-10.8 0.17-0.48 2.4-15 0.9-3.7 15-43 18-53
Mexico
B. pearsei 24-27 916-2963 5.5-8.2 1-14.4 0.09-0.59 0.9-23 0.06-5 9-82 10-86
D. murchiei 24-27 916-2160 7.5-8.9 0.2-2.6 0.06-0.88 1.3-21 0.06-3 22-98 2-74
D. papillata 25-27 814-2130 n.d. n.d. n.d. n.d. n.d. n.d. n.d.
L. parvus 24-27 1156-4725 5.3-8.1 0.9-10.1 0.07-0.42 4.5-17 0.65-11 19-63 13-74
P. taste 19-27 600-2963 5-8 1-14.4 0.08-0.42 4.1-23 0.06-6 9-78 9-86
P. australis 14-25 600-2522 5.3-7.9 1.4-11.8 0.07-0.42 5.6-14 1-6.1 11-63 12-73
R. strigosa 24-27 1000-2963 5-6.5 2.2-6.5 0.11-0.42 4.1-13 1.7-3.6 32-62 9-50
Z. sp.nov 1 24-25 916-1349 7.7-8.3 1.1-7.3 0.02-0.48 0.87-24 0.18-3 9-46 26-62
Ivory Coast
C. palustris 28 1276 5-7 0.75-1.3 0.08-1.3 1.7-2.8 1-2.3 55-82 5-15
C. zielae 28 1276 5-7 0.75-1.3 0.08-1.3 1.7-2.8 1-2.3 55-82 5-15
O. agilis 28 1276 5-7 0.75-1.3 0.08-1.3 1.7-2.8 1-2.3 55-82 5-15
M. anomala 28 1276 5-7 0.75-1.3 0.08-1.3 1.7-2.8 1-2.3 55-82 5-15
Rwanda
E. lavellei n.d. n.d. 3.7-7.4 1.6-4.9 0.08-0.24 n.d. n.d. 32-60 29-54
G.sp1 n.d. n.d. 3.5-7.8 1.4-41.2 0.06-1.4 n.d. n.d. 2-92 10-67
S. variabilis n.d. n.d. 3.7-4.4 3.5-4.7 0.13-0.26 n.d. n.d. 42-85 11-48

T = temperature, DM = organic matter, N = nitrogen, Ca = calcium, Mg = magnesium, 5 = sand, C = clay; ail values from the upper 10 cm
of soil.
16 C. Fragoso et al.

however, are common in tropical agroecosystems (Table 1.4, 31 species in

bold). This group includes species widely distributed at the regionallevel (e.g.
Onychochaeta elegans in Cuba, Balanteodrilus pearsei in southeastern Mexico or
Lampito mauritii in India) or locally abundant (Ramiellona strigosa, Zapatadrilus
sp.nov1 in Mexico and Millsonia anomala in Ivory Coast). Table 1.5 shows the
environmental (precipitation, temperature) and edaphic (pH, organic matter,
nitrogen, sand and clay) tolerance ranges ofsome ofthese species, according to
the country in which they occur. Species listed in this table are those for which
these data were available.

Comparisons between exotic and widely distributed native earthworm

species

So far, we have identified 20 exotic and 27 native species that commonly occur
in tropical agroecosystems of Asia, Arrica and America (Tables 1.2 and 1.5).
Data from Tables 1.3 and 1.5 suggest that these species apparently have wide
ranges of climatic and edaphic tolerances. Figure 1.1 shows that the degree of
tolerance (Le. the environmental plasticity) is larger in the group of exotics,
both at the regional (range of annual precipitation) and locallevel (range of
pH). In this figure, however, environmental plasticity is analysed with range
values (dilTerence between maximum and minimum) ofonly two variables. In
order to determine whether this pattern is maintained with more variables,
two multivariate analyses were performed using the climatic (two) and
edaphic (seven) variables of Tables 1.3 and 1.5. The input matrix consisted of
47 rows (native and exotic species) and nine columns (environmental vari-
ables), data being standardized in both cases. The first analysis was a principal
component analysis (PCA), that ordinated species along two components
which together explained 76% of the total variance (Cl = 62%, C2 = 14%). Cl
and C2 correlated, respectively, with edaphic and climatic ranges. The second
analysis was a cluster analysis, performed using unweighted pair-groups
method analysis (UPGMA) as an average-linkage clustering method. PCA and
UPGMA were made respectively, with STATGRAPHIC and PATN (Belbin, 1976)
software.
Figure 1.2 shows the result of these analyses that ordinated and grouped
the native and exotic species listed in Tables 1.3 and 1.5, into four main
groups:
1. G1 includes those native species with wide edaphic and medium climatic
tolerances (high local plasticity but low regional plasticity), which correspond
to the majority of native widespread Mexican species.
2. G2 are the common exotic species of the tropics that exhibit wide climatic
and edaphic tolerances (high regional and local plasticity).
3. G3 includes species (natives and exotics) with narrow edaphic tolerances
that are resistant to climatic variations (low local but high regional plasticity).
 A Survey of Tropical Earthworms 17

5 Euryoecious

J:
c-
'0
al
Cl
c:
4

3
•
cP
o.
•
• 0
•• .JI
•
•

al 2
a:
• 0 0
•
GD 00
0
. . - Stenoecious

0
0 •
0 1000 2000 3000 4000 5000
Range of precipitation (mm)

o Natives • Exotics

Fig. 1.1. Example of c1imatic (annual precipitation) and edaphic (pH) plasticity of
exotic and native widespread tropical earthworm species. Each point represents a
species. Those situated in the upper right corner indicate euryoecious species,
whereas those situated in the lower left corner indicate stenoecious species. Both
precipitation and pH are range values.

- Climatic plasticity (regional)

Stenoecious

Edaphic plasticity
(local)
+

+
• Exotics D Natives
Fig. 1.2. Ordination (PCA) and c1ustering (UPGMA) of widespread native and
exotic species on the basis of c1imatic and edaphic range values. For initiais see
Table 1.6.
18 C. Fragoso et al.

4. G4 groups species with low tolerance to both climatic and edaphic variables
(low regional and local plasticity). It is this group in which the majority of the
other native species of Table 1.4 should be placed.
Although this analysis is somewhat biased by the amount of records
and/or data available (sorne species have very few records and consequently
low ranges), the output ordination and classification is useful because it pro-
vides a framework for the classification of earthworms with potential for
manipulation, according to their ecological plasticity.
Thus, G2 (euryoecics) includes those exotic species that can be manipu-
lated in the majority of tropical agroecosystems, both if they are introduced
and if they are already present. They represent the species best adapted to
unsuitable edaphic environments: Amynthas gracilis (Ag), A. corticis (Ac),
Dichogaster affinis (Da}), D. bolaui (Dbo), D. saliens (Ds), OcnerodriIus occidentalis
(00), Pontoscolex corethrurus (Pc) and Polypheretima elongata (Pe). The last two
species are endogeic mesohumic species (see Chapter 2 for a defmition of these
terms) which, due to their abundances, cast production and burrowing activi-
ties, have important effects on soil processes. In the same way, GI
(euryedaphic species) corresponds to native species that, for a given country
and/or region, should be ranked frrst in manipulative practices because they
represent the original adapted fauna: BalanteodriIus pearsei (Bp), LaveIIodriIus
parvus (Lpa) , PhoenicodriIus taste (Pt), Diplotrema murchiei (Dm) and
Protozapotecia australis (Pa) in Mexico and HyperiodriIus africanus for several
African countries (this species was not analysed for plasticity, but is very
common in different land-use systems). G3 (stenoedaphic species) comprises
species that could be manipulated in different regions but in the same type of
soil substrate, e.g. epigeic native (Drawida wiIIsii, Dw) and exotic species
(Perionyx excavatus, Pex; BudriIus eugeniae, Be) on organic rich substrates.
Finally, G4 (stenoecic species) represents the more local scale of management:
native species that only survive in a given locality and in a given type of soil.
They might be manipulated at a locallevel, provided no intensive or destruc-
tive practices are used (see Chapter 2). This is the case, for example, for sorne of
the savanna species ofLamto (MiIIsonia anomala, Ma), sorne (but not all) forest
species ofYurimaguas and several Indian (KonkadriIus spI and sp2, Kspl and
Ksp2; Drawida ampullacea, Damp) and Mexican (Ramiellona strigosa, Rs;
ZapatadriIus sp.novI, Zsp) species.
In general, this analysis shows that exotic species are better adapted than
natives to factors that change both at the regional--eontinentallevel (e.g. rain-
fall, temperature) and at the local level (edaphic changes); the majority of
natives, on the other hand, are incapable of adapting to regional variations,
but sorne species are still able to withstand variations at a more locallevel.
Besides environmental plasticity, there are at least two other variables
that could explain the wider distribution of exotics and the absence of native
species in other regions.
 A Survey of Tropical Earthworms 19

1. Parthenogenetic reproduction: almost all exotic species in Table 1.2 are

considered to be facultatively parthenogenetic, meaning that they may
produce viable unfertilized cocoons. Native species in Table lA, on the other
hand, only produce viable cocoons after fertilization (with a few exceptions
such as P. taste and O. elegans). Parthenogenesis, therefore, appears to be an
essential detenninant of the wide geographic distribution of exotics, as was
originally proposed by Reynolds (1974) and Lee (1987). Ifmating is not oblig-
atory, one single individual (even a cocoon) may establish a new population.
2. Historical dispersal by man: the distribution of exotics has been greatly
favoured by the spread of plants worldwide and such practices as the use of soil
as ballast, in thedays oflong sea voyages. Gates (19 72, 1982) intercepted, over
several years, the worms that were introduced to the United States in pots con-
taining imported plants. He found all the exotic species of Table 1.2 and many
native species from several tropical and temperate countries; these species, of
course, did not have any chance to establish in North American soils, but we can
infer that, in the past, this situation occurred repeatedly, being the main cause
for the presence of exotic species.
In sorne cases, it is possible to relate the distribution of sorne exotics to the
origin of introduced plants. The African exotic species Gordiodrilus peguanus
and Eudrilus eugeniae, for example, are present mainly in former European col-
onies (e.g. Greater Antilles; Gates, 1972) that were, in the past, dominated by
an African slave population; they are not present, for example, in Mexico, Peru
and other countries where this population was practically non-existent. In a
number of cases, the absence of euryoecious native species in a given tropical
country may, therefore, better be explained by human activities than by
factors related to ecological plasticity.

Conclusions

The list of most common earthworm species of tropical agroecosystems

includes a set ofeuryoecious exotic species, common in the majority of tropical
countries, and native species that are common for a given country at local or
regionallevels. Table 1.6 lists these species, their ecological categories and the
geographic level at which management of their populations should be
considered.
Most species with potential for manipulation are large species, mainly
mesohumic endogeics and epi-endogeics that live in the soil and ingest a
mixture of soil and surface litter. These species can be considered as ecosystem
engineers because they transfonn the edaphic profile through the production
of casts and burrows; in this regard they are keystone species in the
agroecosystem. Small polyhumic species may play a role in the system (e.g. as
'decompacting' species; see Chapter 5) but may not be crucial in the short term
as their activities do not dramatically affect soil profile and other subordinated
 N
Table 1.G. List of tropical earthworm species with potential for manipulation in an nuaI cropping systems. 0

Species Ecological category Region Management

Oichogaster bolaui (Obo) Epigeic Humid tropics Worldwide

Oichogaster saliens (Os) End. polyhumic Humid tropics Worldwide
Oichogaster affinis (Oaf) End. polyhumic Humid tropics Worldwide
Oichogaster annae (Oann) End. polyhumic Humid tropics Worldwide
Orawida barwelli (Oba) End. polyhumic Humid tropics Worldwide
Eudrilus eugeniae (Ee) Epigeic Humid tropics Worldwide
Metapheretima taprobanae (Mt) End. mesohumic Humid tropics Worldwide
Metaphire califomica (Mc) Epi-endogeic Humid tropics Worldwide
Metaphire houlleti (Mh) Epi-anecic Humid tropics Worldwide 0
Metaphire posthuma (Mp) End. mesohumic Humid tropics Worldwide
Ocnerodrilus occidentalis (Oo) End. polyhumic Humid tropics Worldwide "Ql
~
Periscolex brachycystis (Pb) End. polyhumic Humid tropics Worldwide ln
0
Peryonix excavatus (Pex) Epigeic Humid tropics Worldwide ....CIl
Pheretima bicincta (Pbi) Epi-endogeic Humid tropics Worldwide ~

Polypheretima elongata (Pel) End. mesohumic Humid tropics Worldwide

Pontoscolex corethrurus (Pc) End. mesohumic Humid tropics Worldwide
Balanteodrilus pearsei (Bp) End. Poly-mes. SE Mexico Regional
Oiplotrema murchiei (Dm) End. Poly-mes. SE Mexico Regional
Phoenicodrilus taste (Pt) End. polyhumic SE Mexico Regional
Lavellodrilus parvus (Lpa) End. polyhumic SE Mexico Regional
Protozapotecia australis (Pa) End. polyhumic SE Mexico Regional
Eminoscolex lavellei (El) End. polyhumic Rwanda Regional
Stuhlmannia variabilis (Sv) End. mesohumic Rwanda Regional
Cordiodrilus spl (Cg) End. polyhumic Rwanda Regional
Oichogaster itoliensis (Di) Anecic Rwanda Regional
Onychochaeta elegans (Oe) End. mesohumic Cuba, Caribbean Regional
Onychochaeta windelei (Ow) End. mesohumic Cuba, Caribbean Regional
Pontoscolex spiralis (Ps) End. mesohumic Lower Antilles Regional
Chuniodrilus zielae (Cz) End. polyhumic Lamto, Ivory Coast Regional
Chuniodrilus palustris (Cp) End. polyhumic Lamto, Ivory Coast Regional
Hyperiodrilus africanus (Ha) Epiendogeic Tropical Africa Regional
Lampito mauritii (Lm) Anecic India, SE Asia Regional
Orawida paradoxa (Opa) End. mesohumic Karnataka, India Regional
Orawida ampullacea (Oamp) Endogeic Karnataka, India Regional
Orawida willsii (Ow) Epianecic Karnataka, India Regional
Orawida nepalensis (On) End. mesohumic Karnataka, India Regional
Karmiella karnatakensis (Kk) End. poly-mes. Karnataka, India Regional
Megascolex konkanensis (Mk) Endogeic Karnataka, India Regional
Eutyphoeus incommodus (Ei) Anecic Northern India Regional
Ramiellona strigosa (Rs) End. mesohumic Chiapas, Mexico Local
Zapatadrilus sp.nov (Zsp) Endoanecic Veracruz, Mexico Local
Rhinodrilus pashanasi (Rp) End. mesohumic Peru, Yurimaguas Local
Millsonia anomala (Ma) End. mesohumic lamto, Ivory Coast Local
Millsonia lamtoiana (M/) Anecic Lamto, Ivory Coast Local

....
N
22 C. Fragoso et al.

soil organisms. This aspect, linked to the issue of the functional value of
biodiversity, is considered in Chapters 4 and 5.
The main conclusion of this survey is that native species are found fre-
quently in tropical agroecosystems, particularly in sorne countries (e.g. India)
where apparently low-input agricultural techniques prevail (see Chapter 2 for
more on this point), or in localities with low annual precipitations that do not
permit the invasion of exotics (such as Mexican localities with annual precipi-
tations below 1300 mm, where the native endoanecic Zapatadrilus sp.nov1
dominates and no mesohumic exotics have been able to establish). Taking into
account the fact that several native species survive in agroecosystems at a very
locallevel (Table lA), the number of species to be manipulated in tropical
farming systems turns out to be considerably greater than the 10-15 major
exotic species identified in Table 1.1. In this regard, and at least for tropical
regions, it is no longer possible to maintain Lee's (1987) statement that only
exotic species are important in agriculturallands. In addition, it is highly prob-
able that the number of native species with potential for management in
agroecosystems will increase as a function of the intensity of sampling effort.
So far, we have presented the list of earthworms with potential for manip-
ulation in tropical soils. In agriculturallands, however, manipulation prac-
tiees should be considered at the community level, because mixtures of species
are generally more common than single species. In the next chapter, we will
analyse these species assemblages in relation to their ecological and agricul-
tural determinants and potential for manipulation.

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Library of Congress Cataloging-in-Publication Data

Earthworm management in tropical agroecosystems / edited by P. Lavelle,
L. Brussaard and P. Hendrix.
p. cm.
lncludes bibliographical references and index.
ISBN 0-85199-270-6 (alk. paper)
1. Earthworm culture -- Tropics. 2. Earthworms -- Ecology -- Tropics. 1.
Lavelle, P. (Patrick) Il. Brussaard, L. (Lijbert) III. Hendrix, Paul F.
SF597.E3E27 1999
639'.75--dc21 99-12081
OP
ISBN 0 851992706

Typeset by AMA OataSet Ud, UK

Printed and bound in the UK by Biddles Ud, Guildford and King's Lynn