Regeneration in Annelids
Mark J Zoran, Texas A&M University, College Station, Texas, USA
Annelids, like many other invertebrate animals, replace
lost body parts in a process called regeneration. However,
the ability to regenerate lost segments is present in some
groups and not others, for example leeches do not
regenerate lost segments. Anterior and posterior regen-
eration involves the formation of a bud containing stem
cells that differentiate into the new head or tail segments.
Annelid regeneration also involves remodelling of sur-
viving body fragments. The ability of annelids to regen-
erate tail segments appears to be nearly universal among
species capable of regeneration. The ability to regenerate
head segments, although common, is not universal and
can depend on the number of segments lost. The absence
and presence of regeneration across annelid groups,
including closely related species, suggests that regener-
ation ability may be an ancient trait that has been lost in
some species during annelid evolution. Why regeneration
varies among annelid species remains an intriguing
question for life scientists.
Introduction
Regeneration is the process of repairing or replacing
damaged or lost body parts following injury, a mechanism
that varies considerably among animal groups (Sanchez
Alvarado and Tsonis, 2006). Flatworms, for example,
regenerate entire new bodies from a small amputated part.
Still other animal groups, like birds and mammals, have
little or no capacity for regenerating their bodies. Similarly,
some annelids, like leeches, cannot regenerate lost body
ELS subject area: Developmental Biology
How to cite:
Zoran, Mark J (September 2010) Regeneration in Annelids. In:
Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Ltd: Chichester.
DOI: 10.1002/9780470015902.a0022103
ENCYCLOPEDIA OF LIFE SCIENCES & 2010, John Wiley & Sons, Ltd. www.els.net
Advanced article
Article Contents
. Introduction
. Segmental Regeneration in Annelids
. Morphallactic Regeneration in Annelids
. ‘Regeneration’ during Asexual Reproduction
. Other Forms of Regeneration in Annelids
. Evolution of Annelid Regenerative Abilities
. Conclusions
Online posting date: 15th September 2010
parts. Nonetheless, the majority of annelid taxonomic
groups contain species capable of regeneration. See also:
Regeneration: Principles
Annelids are metameric, meaning they are segmental
animals composed of repeated body parts. Although
anterior segments can each be specific in their structure,
containing brain ganglia or reproductive structures, the
vast majority of segments are replicated parts containing
similar organ structure. Therefore, the loss of anterior
segments and their subsequent replacement may be more
costly than the regeneration of posterior segments. Among
oligochaete annelids, terrestrial species generally emerge
head first from their burrows. In contrast, most aquatic
oligochaetes live with their heads burrowed into the sub-
strate and their tails extending up into the water, as tail
segments are often adapted for gas exchange. Thus,
earthworms are especially vulnerable to predatory attacks
directed towards anterior segments, whereas tubificid and
some lumbriculid worms have likely been subjected to
predominately tail-directed attacks (Zoran and Drewes,
1987; Zoran et al., 1988; Zoran and Martinez, 2009). Given
this, we might expect terrestrial and aquatic oligochaetes to
possess differential abilities for anterior and posterior
segmental regeneration, respectively. This is not the case, as
posterior regeneraton is basically universal among oligo-
chaetes (Bely, 2006). However, head regeneration among
annelid worms is much more variable.
Why animals vary in their ability to regenerate is a long-
standing question in biology (Morgan, 1901). A number of
animal regeneration models exist that address the devel-
opmental and molecular mechanisms of this process. These
include studies of body part restoration in hydra, planar-
ians and amphibians. Although many annelid species
possess the ability to regenerate body parts, regeneration is
a highly variable trait among annelid groups and it presents
itself in diverse contexts. Along with segmental regener-
ation following injury, annelids have marked capacities for
regeneration following fragmentation associated with
asexual reproduction and with self-fragmentation by
autotomy. These varied contexts for regeneration are pre-
sent in some annelids and not others, whereas different
regenerative abilities exist among closely related species.
This review constitutes a general overview of the
1
 Regeneration in Annelids

Aeolosoma Enchytraeus
Arenicola* Lumbriculus
Owenia Lumbricus
Myxicola* Paranais*
Sabella Tubifex Branchiobella* Hirudo*

Branchiobdellida
Hirudinida
Oligochaeta

Polychaeta

Clitellata

Annelid
phylogeny

Burrowing
marine worm
Figure 1 Phylogenetic variation in annelid segmental regeneration. Annelids are thought to have evolved from a burrowing marine ancestor that likely was
able to regenerate lost body parts. During annelid evolution, the ability to regenerate, particularly head segments, has been lost (and possibly gained) in
several groups. Hirudinids (leeches) and the closely related Branchiobdellida cannot regenerate lost segments, whereas many polychaetes and oligochaetes
do so readily. Genera names in red () indicate annelid groups that contain species unable to regenerate lost heads. Genera names in green indicate annelid
groups that contain species that can regenerate these lost anterior body segments.

regenerative capabilities of annelid worms. It is based
largely on a series of classic analyses of the subject con-
ducted many decades ago, including Hyman (1940), Berrill
(1952) and Herlant-Meewis (1964). Additionally, this
review incorporates modern research, including an excel-
lent survey of annelid regeneration by Bely (2006). See also:
Regeneration in Planaria; Regeneration of the Urodele
Limb
Segmental Regeneration in Annelids
The ability to regenerate lost body segments varies widely
across annelid phylogeny (Figure 1). Leeches, and perhaps
their close allies the branchiobdellids, are completely
incapable of segmental regeneration (Hyman, 1940; Bely,
2006). Similarly, some polychaetes, such as Arenicola
marina, are thought to be incapable of either anterior or
posterior regeneration (Wells, 1966). Nonetheless, the
ability to replace lost body parts is a far more common
feature of this animal phylum than the alternative lack of
regeneration. In fact, some sabellid, chaetopterid and
lumbriculid species are capable of regenerating an entire
individual from one or a few segments (Morgulis, 1907;
Berrill, 1928). This form of segmental regeneration
involves the activation of stem cell populations to form a
blastema and subsequent segmental bud. This bud of stem
cells growing from the original body fragment then
develops into the new head or tail segments. This regen-
erative process is called epimorphic regeneration. Epi-
morphosis is the de-differentiation of extant tissues
followed by generation of new body tissues requiring
on-going cell division and differentiation (Morgan, 1901;
Goss, 1969). See also: Regeneration Model Systems:
Invertebrate Epimorphic
Interestingly, very closely related species, including ani-
mals within the same genera, have striking differences
in regenerative capability. For example, Myxicola anesthe-
tica reportedly regenerates lost anterior segments; whereas
Myxicola infundibulum, like the leeches, is thought to have
no head or tail regeneration ability (Wells, 1952). Although
these two fanworm species and some other polychaete
groups, including nereid worms, have a reduced potential
for anterior segment regeneration (Bely, 2006), many other
polychaete groups, such as spionid worms, possess the
ability to regenerate anterior body segments quite effectively
(Lindsay et al., 2007, 2008). Still, the oft-quoted idea that
anterior segment regeneration is rare among annelids is
flatly inaccurate. Rather, head segment regeneration is
widespread, particularly among oligochaete groups.
Earthworms, including Eisenia foetida and Lumbricus ter-
restris, and freshwater worms, such as Limnodrilus claper-
edianus and Tubifex tubifex, are known to regenerate lost
head segments. Still, other oligochaete species, like the
tubificid Paranais litoralis, are not able to replace lost head
segments (Bely, 1999). It should be noted, however, that
even among species with documented head regeneration
ability, the extent of that capability often varies according to
the position of the fragmentation site along the anterior–
posterior axis or the number of head segments lost to injury
(Hyman, 1940; Berrill, 1952; Herlant-Meewis, 1964). For
example, in the lumbricid worm, E. foetida, regeneration of
anterior structures is significantly reduced as more segments
are removed. This species is not capable of anterior

2 ENCYCLOPEDIA OF LIFE SCIENCES & 2010, John Wiley & Sons, Ltd. www.els.net
 Regeneration in Annelids

regeneration when greater than 20 anterior segments are
removed (Berrill, 1928, 1952). In contrast, the lumbriculid
mudworm, Lumbriculus variegatus, stereotypically regen-
erates a restricted, yet precise number of 7–8 head segments
regardless of the fragmentation site along the animal’s body
axis or the number of body segments removed (Morgulis,
1907; Drewes and Fourtner, 1990).
The ability to regenerate body segments via epimor-
phosis is thought to have been lost multiple times during
annelid evolution (Bely and Nyberg, 2010). In fact, a broad
analysis of head regeneration among naidine worms shows
that at least 14 species possess the capacity for head res-
toration, whereas some 6 species cannot mount such a
regenerative response (Bely and Sikes, 2010). Phylogenetic
analyses suggest that head regeneration has been lost on
three occasions among this group of closely related aquatic
oligochaetes. Berrill (1952) observed that the blastema of
regenerating annelids combines both the de-differentiation
of mature segmental tissues and the differentiation of newly
generated stem cell populations. Whether this is a universal
trait among annelids remains to be seen, nonetheless, the
blastema is critical for epimorphic segmental regeneration.
In fact, among several annelid groups that lack segmental
regeneration, wound healing occurs normally but the fail-
ure of a blastema to form creates a block to regeneration
(Bely, 2006; Bely and Nyberg, 2010).
Thus, annelid regeneration is widespread and diverse. It
is present across broad taxonomic groups, whereas missing
in others. Many polychaete and oligochaete species replace
their lost heads, whereas almost all of these species regen-
erate their lost tails. Segmental regeneration in annelids is
often a graded response depending on the extent of the
body injury, yet in some species this process is rigidly
regulated and largely independent of the number of
segments lost. How this variation in regeneration is
accomplished may lie in the cellular and molecular mech-
anisms governing blastema formation. Why regeneration is
variable across the annelid phylogeny remains a mystery
and is discussed further in the following text.
Morphallactic Regeneration in
Annelids
The process of epimorphic segmental regeneration is
accompanied by morphallactic regeneration in the sur-
viving (original) body fragment of some polychaete species,
such as Sabella pavonina (Berrill, 1978) and the some
oligochaete species, like Enchytraeus japonensis (Takeo
et al., 2008). Morphallaxis is a pattern of regeneration that
involves the transformation of existing tissues with no
significant stem cell differentiation (Holstein et al., 2003).
As recent cellular and molecular studies have identified
some mechanisms of regeneration across diverse species,
the utility of the terms epimorphosis and morphallaxis has
been called into question (Agata et al., 2007). These
authors argue that investigating how positional identity is
rearranged and what type of cells contributes to this
reorganisation is most important. Further, the terms
themselves may limit our understanding of the processes.
Unlike animals that regenerate largely by one or the other
classical forms of regeneration, annelid fragments that
survive injury often transform into newly organised seg-
ments possessing new positional identities through the
combined mechanisms of epimorphic bud formation and
morphallactic segment reorganisation (Bely and Nyberg,
2010; Berrill, 1952; Drewes and Fourtner, 1990; Myohara

Anterior
Head bud Morphallaxis
Blastema

Tail bud

Epimorphosis
Fragment 2 weeks

Posterior

Figure 2 Regeneration in the oligochaete worm Lumbriculus variegatus. Following injury and wound healing, a blastema is formed on both the anterior and
posterior ends of the fragment. Over a two-week period, head and tail buds are generated from blastema-derived stem cells in a regenerative process called
epimorphosis. Concurrently, tissues of the original body segments undergo a reorganisation of their physiology and anatomy, in the absence of new stem
cell differentiation, in a regenerative process called morphallaxis. Anterior epimorphosis in this species produces a head of only 7–8 segments. Thus,
segments of the posterior fragment isolated from the injured animal on the left become anterior segments of the new animal on the right.

ENCYCLOPEDIA OF LIFE SCIENCES & 2010, John Wiley & Sons, Ltd. www.els.net 3
 Regeneration in Annelids
et al., 2006). Figure 2 illustrates the combined nature of
regeneration in the aquatic oligochaete L. variegatus. In
this species, head and tail segments are replaced on injured
fragments via epimorphosis, and original body segments
are reorganised to match new regional identities via mor-
phallaxis (Martinez et al., 2005; Zoran and Martinez,
2009).
The prevalence of morphallaxis among oligochaetes is
unknown. Besides the sabellid and enchytraeid species
mentioned in the preceding text, morphallactic mech-
anisms have been described in L. variegatus (Drewes and
Fourtner, 1990) and E. foetida (Chapron, 1970). The cel-
lular, molecular, anatomical and physiological substrates
of morphallaxis are emerging in two oligochaete species:
E. japonensis (Myohara et al., 1999; Yoshida-Noro et al.,
2000; Myohara, 2004; Müller, 2004; Takeo et al., 2008) and
L. variegatus (Drewes and Fourtner, 1990; Martinez et al.,
2005; Zoran and Martinez, 2009). Since epimorphic
regeneration of body segments is widespread in this phy-
lum, morphallaxis may also be a common annelid trait –
but largely unexamined and thus underreported.
The lumbriculid worm L. variegatus exhibits anterior–
posterior gradients in behaviour (Lesiuk and Drewes,
2001). Tactile stimuli in the anterior one-third of the
worm’s body elicit head withdrawal (Drewes, 1984; Zoran
and Drewes, 1987). Conversely, stimulation of the pos-
terior two-third of the worm results in tail shortening. As
aforementioned, L. variegatus fragments regenerate only
eight head segments and varying numbers of posterior
segments. Thus, following regeneration, original posterior
segments often become more anterior in the new body
configuration. This change in positional identity coincides
with morhallactic (anatomical and physiological) changes.
These transformations are especially interesting in the
nervous system, where this process is called neural mor-
phallaxis (Drewes and Fourtner, 1990; Martinez et al.,
2005). Neural morphallactic changes in L. variegatus
involve changes of neural sensory fields and the expression
of morphallaxis-specific proteins in the surviving segments
(Zoran and Martinez, 2009). Interestingly, these proteins
are enriched on the very neuronal axons and synapses that
are involved in the sensory field changes (Martinez et al.,
2005). Therefore, morphallactic mechanisms in annelids
might involve cellular changes not unlike the neural
mechanisms that govern other adaptive forms of behav-
ioural plasticity, like learning and memory.
‘Regeneration’ during Asexual
Reproduction
Annelids generally have a marked capacity for wound
healing. For example, even though leeches do not regen-
erate lost segments, they generate an effective response to
injury by assembling an extracellular protein scaffold that
facilitates the restoration of tissues (Tettamanti et al.,
2005). Although wound healing and regeneration often go
4 ENCYCLOPEDIA OF LIFE SCIENCES & 2010, John Wiley & Sons, Ltd. www.els.net
hand-in-hand, in some regenerative contexts wound heal-
ing is neither needed nor present. This is the case in
regeneration associated with some forms of asexual fission.
Here, internal programmes for regeneration are activated
such that fragmentation proceeds in a prolonged and
regulated process. In L. variegatus, for example, cellular
and molecular changes in segmental physiology occur days
to weeks before fission planes are formed, fragmentation
occurs and the sister zooids are physically separated
(Martinez et al., 2006). Once fission occurs, little if any
wound healing is necessary. In Dero digitata, asexual
reproduction involves body fission, which separates the
worm into anterior and posterior zooids. Four new head
segments are developed by the posterior zooid and many
new tail segments are generated by the anterior zooid
(Drewes and Fourtner, 1991).
This ability to asexually reproduce through an endo-
genously induced process of body fission is reported for
nine polychaete (Schroeder and Hermans, 1975) and four
oligochaete families (Brinkhurst and Jamieson, 1971).
Interestingly, some species capable of this form of repro-
ductive regeneration, such as the naidid worm, P. litoralis,
are incapable of regeneration following body amputation
outside the context of reproduction (Bely, 1999). This rai-
ses an important question. If a worm can reproduce
asexually, but cannot regenerate following injury, is
body restoration (epimorphosis-like processes) or body
reorganisation (morphallaxis-like processes) that occurs
during asexual reproduction truly regeneration? If during
asexual fission no blastema is formed, then can classically
defined epimorphosis occur? Comparison of gene expres-
sion data indicates large similarities in the genetic regu-
lation of regeneration, asexual fission and embryonic
processes (Bely and Wray, 2001). Thus, annelid fission may
have evolved by recruitment of extant regenerative pro-
cesses, which are themselves a re-deployment of processes
shared with embryonic development.
One intriguing question regarding regeneration in
annelids, particularly those that form entire animals from a
few segments, is how do fragments that contain no gonads
give rise to sexually mature worms that can produce viable
cocoons? As it turns out, specific cells are distributed
throughout the body of the oligochaete worm, E. japo-
nensis, which serve as reservoirs of germ-cell precursors
(Tadakoro et al., 2006). During regeneration, these cells
differentiate, proliferate and regenerate new gonads. Thus,
the regeneration of gonad is accomplished in any zooid
derived from any body fragment produced by asexual
fission.
Other Forms of Regeneration in
Annelids
Along with internally regulated asexual fission, many
oligochaetes are able to self-fragment by autotomy in
response to noxious stimulation (Lesiuk and Drewes,

1999). In these cases, fragmentation is also induced
internally, but is not regulated by developmental pro-
grammes. Rather, these noxious stimuli activate reflexes
that trigger acute contractions of specific body muscles that
force the body to fragment. Thus, segmental separation by
autotomy is quite distinct from fragmentation by asexual
fission. Since we defined regeneration at the outset as the
process of replacing lost body parts following injury, then
this process is clearly regeneration – the fact that the injury
here is self-inflicted notwithstanding.
Annelids have also evolved several novel forms of com-
pensatory regeneration that do not involve replacement of
existing segments. For example, the lugworm, A. marina,
and the tubificid worm, Branchiura sowerbyi, are both
burrowing annelids, a marine polychaete and a freshwater
oligochaete, respectively. Although extremely distant in
phylogenetic terms, their tails are both subjected to fre-
quent predation and segmental loss. Arenicola, which does
not regenerate posterior segments, expands the size of its
remaining segments to compensate for lost tissue (De Vlas,
1979). Although not technically a form of regeneration,
this is a novel adaption for the recovery of behavioural
function. Branchiura, however, which exhibits robust
regeneration of its gill-bearing posterior segments when
lost to predation, also generates a transient differentiation
of the most posterior of its remaining tail segments, such
that a pair of gill filaments is generated on each segment,
presumably to compensate for temporary loss in gas-
exchange capacity (Drewes and Zoran, 1989).
Finally, annelids regenerate specific body tissues, for
example their nervous systems, rapidly and accurately after
tissue trauma. Studies of neural regeneration have focused
largely on the injured central nervous system in earth-
worms (Drewes et al., 1988). For example, in L. terrestris,
regenerating giant interneurons show a high degree of
specificity in establishing new contacts with their appro-
priate partners (Birse and Bittner, 1976, 1981). This
recovery of function is also rapid, less than 24 h after ven-
tral nerve cord crush and only days following transection of
the nerve cord (Drewes et al., 1988).
Evolution of Annelid Regenerative
Abilities
The regeneration of lost body parts is widespread among
basal metazoan lineages (Bely and Nyberg, 2010). This
understanding, together with the knowledge that anterior
and posterior segmental regeneration is common among
annelids, has led to the speculation that these regenerative
capabilities are ancestral traits to this phylum (Bely, 2006).
By extension, the ability to regenerate must have been lost
during annelid evolution multiple times. This idea is sup-
ported, as aforementioned, that head regeneration has
been lost three times in the naidine phylogeny (Bely and
Sikes, 2010). The lumbriculid worms are thought to rep-
resent an oligochaete group ancestral to, or at least closely
ENCYCLOPEDIA OF LIFE SCIENCES & 2010, John Wiley & Sons, Ltd. www.els.net
Regeneration in Annelids
related to, the leeches (hirudinids) and the branchiobdellid
worms (Brinkhurst and Gelder, 1989). It is surprising then
that lumbriculid species possess marked abilities for both
head and tail regeneration, whereas no hirudinid or bran-
chiobdellid examples of segmental regeneration exist.
Therefore, it may be that leeches and their allies have lost
regenerative abilities that were present in ancestral lin-
eages. Furthermore, mechanisms of regeneration have
been lost recently in some annelid groups (Bely, 2006).
Unfortunately, the evolutionary relationships among
annelids are largely unresolved. Current ideas posit that the
Clitellata (oligochaetes and leeches) represent a phylo-
genetic group derived within Polychaeta. Furthermore,
groups of unsegmented worms (Echiura and Sipuncula)
and worms with modified segmentation (Siboglinidae=
Pogonorphora) are annelids derived from polychaete
ancestors (Struck et al., 2007; Bleidorn, 2009). Virtually
nothing is known of the regenerative capabilities of these
worms, with the exception of reported ‘regeneration’ fol-
lowing asexual reproduction in a sipunculid species (Rice,
1970). Consequently, the evolutionary implications of
regeneration among annelids remain obscure, as do much
of the mechanistic relationships between wound healing,
epimorphic and morphallactic regeneration. Nonetheless,
the diversity of regeneration within the annelid phylogeny
provides a rich substrate on which these problems might be
resolved. See also: Annelida (Segmented Worms); Echiura
(Unsegmented Protostome Worms); Pogonophora (Beard
Worms); Sipuncula (Unsegmented Marine Worms)
Conclusions
Bely and Nyberg (2010) raise the possibility that, based on
the phylogenetic distribution of metazoan regeneration,
regeneration arose in early animals, perhaps along with the
origin of mulicellularity. Therefore, as body parts became
specialised and necessary for success of the whole organ-
ism, a capacity to replace them when lost coincidently
evolved. Annelids clearly have impressive abilities for
regenerating lost body parts. Posterior segment regener-
ation is particularly robust and widespread, although
anterior segment regeneration is not uncommon. Annelid
regeneration involves broad developmental, cellular and
molecular, neural and behavioural mechanisms, many of
which are being elucidated using model species of naidines,
enchytraeds and lumbriculids. These include wound heal-
ing, compensatory growth, and epimorphic and mor-
phallactic mechanisms. Although the evolutionary
relationships between these forms of regeneration in
annelids remain unresolved, it is likely that multiple losses,
and perhaps gains, in regeneration ability have occurred
during annelid evolution.
The capacity for regeneration among annelids, besides
being an interesting developmental, behavioural and evo-
lutionary issue, has ecological importance. Some poly-
chaetes (De Vlas, 1979; Lindsay et al., 2008), and likely
some oligochaetes (Zoran and Drewes, 1988), that
5
 Regeneration in Annelids
frequently lose and replace body parts may provide sig-
nificant sources of renewable biomass for grazing preda-
tors such as fishes and birds. Annelids life cycles include
sexual reproduction via cocoons, asexual reproduction
involving the formation of zooid clones, injury-induced
fragmentation associated with segmental regeneration,
and self-fragmentation and regeneration during rapid
autotomy. The ecological impacts of these widespread
regenerative behaviours to terrestrial, freshwater and
marine communities remain ill understood and largely
neglected. Perhaps, with renewed interests in ecology,
evolution and conservation, combined with new life science
tools, the discovery of the ecological impact of annelid
regeneration is close at hand.
References
Agata K, Saito Y and Nakajima E (2007) Unifying principles of
regeneration I: epimorphosis versus morphallaxis. Develop-
ment, Growth and Differentiation 49: 73–78.
Bely AE (1999) Decoupling of fission and regeneration capabil-
ities in an asexual oligochaete. Hydrobiologia 406: 243–251.
Bely AE (2006) Distribution of segment regeneration ability in the
Annelida. Integrative and Comparative Biology 46: 508–518.
Bely AE and Nyberg KG (2010) Evolution of animal regener-
ation: re-emergence of a field. Trends in Ecology and Evolution
25: 161–170.
Bely AE and Sikes JM (2010) Latent regeneration abilities persist
following recent evolutionary loss in asexual annelids. Pro-
ceedings of the National Academy of Sciences of the USA 107:
1464–1469.
Bely AE and Wray GA (2001) Evolution of regeneration and
fission in annelids: insights from engrailed- and orthodonticle-
class gene expression. Development 128: 2781–2791.
Berrill NJ (1928) Regeneration in the polychaete Chaetopterus
variopedatus. Journal of Marine Biological Association of the
United Kingdom 15: 151–158.
Berrill NJ (1952) Regeneration and budding in worms. Biological
Review 27: 401–438.
Berrill NJ (1978) Induced segmental organization in sabellid
worms. Journal of Embryology and Experimental Morphology
47: 85–96.
Birse SC and Bittner GD (1976) Regeneration of giant axons in
earthworms. Brain Research 113: 575–581.
Birse SC and Bittner GD (1981) Regeneration of earthworm giant
axons following transection or ablation. Journal of Neuro-
physiology 45: 724–742.
Bleidorn C (2009) Annelid phylogeny – molecular analysis with an
emphasis on model annelids. In: Shain DH (ed.) Annelids in
Modern Biology, pp. 13–30. Hoboken, NJ: Wiley.
Brinkhurst RO and Gelder SR (1989) Did the lumbriculids pro-
vide the ancestors of the branchiobdellidans, acanthobdellidans
and leeches? Hydrobiologia 180: 7–15.
Brinkhurst RO and Jamieson BGM (1971) Aquatic Oligochaeta of
the World. Toronto: University of Toronto Press.
Chapron C (1970) Study in oligochaetous Eisenia foetida of
morphallaxis phenomena which are demonstrated in the pre-
vious digestive duct during cephalic regeneration. Comptes
6 ENCYCLOPEDIA OF LIFE SCIENCES & 2010, John Wiley & Sons, Ltd. www.els.net
Rendus Hebdomadaires des Seances de l Academie des Sci-
ences. D: Sciences Naturelles D270: 1362–1364.
De Vlas J (1979) Secondary production by tail regeneration in a
tidal flat population of lugworms (Arenicola marina), cropped
by flatfish. The Netherlands Journal of Sea Research 13:
362–393.
Drewes CD (1984) Escape reflexes in earthworms and other
annelids. In: Eaton RC (ed.) Neural Mechanisms of Startle
Behavior, pp. 43–91. New York: Plenum Press.
Drewes CD and Fourtner CR (1990) Morphallaxis in an aquatic
oligochaete, Lumbriculus variegatus: reorganization of escape
reflexes in regenerating body fragments. Developmental Biology
138: 94–103.
Drewes CD and Fourtner CR (1991) Reorganization of escape
reflexes during asexual fission in an aquatic oligochaete, Dero
digitata. Journal of Experimental Zoology 260: 170–180.
Drewes CD, Vining EP and Zoran MJ (1988) Regeneration of
rapid escape reflex pathways in earthworms. American Zoolo-
gist 28: 1077–1089.
Drewes CD and Zoran MJ (1989) Neurobehavioral special-
izations for respiratory movements and rapid escape from
predators in posterior segments of the tubificid Branchiura
sowerbyi. Hydrobiologia 180: 65–71.
Goss RJ (1969) Principles of Regeneration. New York: Academic
Press.
Herlant-Meewis H (1964) Regeneration in annelids. Advances in
Morphogenesis 4: 155–215.
Holstein TW, Hobmayer E and Technau U (2003) An evo-
lutionarily conserved model system of regeneration? Develop-
mental Dynamics 226: 257–267.
Hyman LH (1940) Aspects of regeneration in annelids. American
Naturalist 74: 513–527.
Lesiuk NM and Drewes CD (1999) Autotomy reflex in a fresh-
water oligochaete, Lumbriculus variegatus (Clitellata: Lum-
briculidae). Hydrobiologia 406: 253–261.
Lesiuk NM and Drewes CD (2001) Behavioral plasticity and
central regeneration of locomotor reflexes in the freshwater
oligochaete, Lumbriculus variegatus. I. Transection studies.
Invertebrate Biology 120: 248–258.
Lindsay SM, Jackson JL and Forest DL (2008) Morphology of
anterior regeneration in two spionid polychaete species: impli-
cations for feeding efficiency. Invertebrate Biology 127: 65–79.
Lindsay SM, Jackson JL and He SQ (2007) Anterior regeneration
in the spionid Polychaetes, Dipolydora quadrilobata and
Pygospio elegans. Marine Biology 150: 1162–1172.
Martinez VG, Menger GJ III and Zoran MJ (2005) Regeneration
and asexual reproduction share common molecular changes:
upregualtion of a neural glycoepitope during morphallaxis in
Lumbriculus. Mechanisms of Development 122: 721–732.
Martinez VG, Reddy PK and Zoran MJ (2006) Asexual repro-
duction and segmental regeneration, but not morphallaxis, are
inhibited by boric acid in Lumbriculus variegatus (Annelida:
Clitellata: Lumbriculidae). Hydrobiologia 564: 73–86.
Morgan TH (1901) Regeneration. New York: Macmillan.
Morgulis S (1907) Observations and experiments on regeneration
in Lumbriculus. Journal of Experimental Zoology 4: 549–574.
Müller MCM (2004) Nerve development, growth and differen-
tiation during regeneration in Enchytraeus fragmentosus and
Stylaria lacustris (Oligochaeta). Development Growth and Dif-
ferentiation 46: 471–478.

Myohara M (2004) Differential tissue development during
embryogenesis and regeneration in an Annelid. Developmental
Dynamics 231: 349–358.
Myohara M, Niva CC and Lee JM (2006) Molecular approach to
annelid regeneration: cDNA subtraction cloning reveals vari-
ous novel genes that are upregulated during the large-scale
regeneration of the oligochaete, Enchytraeus japonensis.
Developmental Dynamics 235: 2051–2070.
Myohara M, Yoshida-Noro C, Kobari F and Tochinai S (1999)
Fragmenting oligochaete Enchytraeus japonensis: a new
material for regeneration study. Development Growth Differ-
entiation 41: 549–555.
Rice ME (1970) Asexual reproduction in a sipunculan worm.
Science 167: 1618–1620.
Sanchez Alvarado A and Tsonis PA (2006) Bridging the regen-
eration gap: genetic insights from diverse animal models.
Nature Reviews. Genetics 7: 873–884.
Schroeder PC and Hermans CO (1975) Annelida: Polychaeta. In:
Giese AC and Pearse JS (eds) Reproduction of Marine Inverte-
brates, Vol. 3. Annelids and Echiurans, pp. 1–213. New York:
Academic Press.
Struck TH, Schult N, Kusen T et al (2007) Annelid phylogeny and
the status of Sipuncula and Echiura. BMC Evolutionary Biology
7: 57–68.
Tadakoro R, Sugio M, Kutsuna J, Tochinai S and Takahashi Y
(2006) Early segregation of germ and somatic lineages during
gonadal regeneration in the annelid Enchytraeus japonensis.
Current Biology 16: 1012–1017.
Takeo M, Yoshida-Noro C and Tochinai S (2008) Morphallactic
regeneration as revealed by region-specific gene expression in
the digestive tract of Enchytraeus japonensis (Oligochaeta,
Annelida). Developmental Dynamics 237: 1284–1294.
Tettamanti G, Grimaldi A, Congiu T et al (2005) Collagen
reorganization in leech wound healing. Biology of the Cell 97:
557–568.
Wells GP (1952) The respiratory significance of the crown in the
polychaete worms Sabella and Myxicola. Proceedings of the
Royal Society of London, Series B 140: 7082.
ENCYCLOPEDIA OF LIFE SCIENCES & 2010, John Wiley & Sons, Ltd. www.els.net
Regeneration in Annelids
Wells GP (1966) The lugworm (Arenicola) – a study in adaptation.
The Netherlands Journal of Sea Research 3: 294–313.
Yoshida-Noro C, Myohara M, Kobari F and Tochinai S (2000)
Nervous system dynamics during fragmentation and regener-
ation in Enchytraeus japonensis (Oligochaeta, Annelida).
Development Genes and Evolution 210: 311–319.
Zoran MJ and Drewes CD (1987) Rapid escape reflexes in aquatic
oligochaetes: variations in design and function of evolutionary
conserved giant fiber systems. Journal of Comparative Physiol-
ogy A 161: 729–738.
Zoran MJ and Drewes CD (1988) The rapid tail withdrawal reflex
of the tubificid worm, Branchiura sowerbyi. Journal of Experi-
mental Biology 137: 487–500.
Zoran MJ, Drewes CD, Fourtner CR and Siegel AJ (1988) The
lateral giant fibers of the tubificid worm, Branchiura sowerbyi:
structural and functional asymmetry in a paired interneuronal
system. Journal of Comparative Neurology 275: 76–86.
Zoran MJ and Martinez VG (2009) Lumbriculus variegatus and
the need for speed: a model system for studies of rapid escape,
regeneration and asexual reproduction. In: Shain DH (ed.)
Annelids in Modern Biology, pp. 185–202. Hoboken, NJ: Wiley.
Further Reading
Carlson BM (2007) Principles of Regenerative Biology. London:
Elsevier.
Dinsmore CE (1991) A History of Regeneration Research: Mile-
stones in the Evolution of a Science. New York: Cambridge
University Press.
Dinsmore CE and Mescher AL (1998) The role of the nervous
system in regeneration. In: Ferretti J and Geraudie J (eds)
Cellular and Molecular Basis of Regeneration, pp. 79–108.
Chichester: Wiley.
Goss RJ (1992) The evolution of regeneration: adaptive or
inherent? Journal of Theoretical Biology 159: 241–260.
7