The effect of amputation of polymelic walking legs and of parts of appendage complexes in Tegenaria atrica (Araneae: Agelenidae)

2006·0.21 MB·English

by  Napiorkowska, T

Bull.Br.arachnol.Soc.(2006)13(9),347–352 347
The effect of amputation of polymelic walking legs studying the epimorphic regeneration of appendages in
and of parts of appendage complexes in Tegenaria the initial stages of postembryogeny in Tegenaria atrica
atrica (Araneae: Agelenidae) C. L. Koch (Agelenidae).
Other arachnologists who have studied the capability
TeresaNapiórkowska,LechJacun´skiandJulitaTemplin for appendage regeneration include Friedrich (1906),
Weiss (1907), Oppenheim (1908), Wood (1926),
DepartmentofInvertebrateZoology,
InstituteofGeneralandMolecularBiology, Gabritschevsky (1927, 1930), Bonnet (1930), Locket
NicolausCopernicusUniversity, (1936), Savory (1936), Ruhland (1976), Randall (1981),
Gagarina9,87-100Torun´,Poland Roth & Roth (1984) and Vollrath (1990). According to
these authors epimorphosis of the feeding and walking
Summary appendages of the prosoma is a common phenomenon,
and as long as the spider is capable of moulting it can
Experimentsontheepimorphiccapabilitiesofpolymelic
regenerateitslostappendages.Moreover,itiscapableof
walking appendages and those forming so-called complex
carrying out regenerative action repeatedly in its
anomaliesinTegenariaatricaC.L.Kochwerecarriedout
intwostages.Firsttheappropriatechangesinthestructure postembryonic life. Simultaneous re-creation of frag-
oftheprosomawereinducedusingtheteratogeniceffectof mentsofseveralappendagesisalsopossible,irrespective
alternating temperatures (14 and 32(C, changing every ofthelocationofamputation.Theobservationsofthese
12h)ondevelopingembryos.Secondly,somefragmentsof
researchers were concerned mainly with appendages of
the deformed appendages were amputated using steelon
normal anatomical structure, which had developed in
threadligaturesinordertoobservethesuccessivephasesof
the regeneration process. Until the termination of the undisturbed ontogeny. Therefore, the question arises
experiments, no external regenerates were found on the whether polymelic appendages and those that are parts
post-amputationsurfacesinanyoftheoperatedindividuals. of complicated appendage complexes have similar epi-
morphic capabilities. Such anomalies can develop as
a result of teratogenic factors acting on developing
Introduction
embryos.
Inspiders,asinotherarthropodsbelongingtovarious One of these factors is temperature. Its teratogenic
systematic taxa, there occur processes of epimorphic effect was noticed by Holm (1940), who described
regeneration. This mode of regeneration can be defined dichotomy of the prosoma in Aranea sexpunctata (L.)
in most general terms as the re-creation of a part of the (=Nuctenea umbratica (Clerck)) and reduction of the
body at the place of its loss or injury without the opisthosoma in Tapinopa longidens (Wider), and
necessity of reorganising the whole organism (Jura & Juberthie (1962, 1963a, b, 1968), who studied the effect
Krzanowska, 1998). In arthropods epimorphosis occurs ofincreasedtemperatureontheembryonicdevelopment
mainly in the appendages, which owing to their jointed ofOpiliones.Similarly,Jacun´ski(1969,1971),Mikulska
structure have become convenient material for compre- (1973) and Mikulska & Jacun´ski (1970, 1971) induced
hensive studies of these processes. It is possible to carry developmental monstrosities in Argyroneta aquatica
out comparative anatomical analysis of the developed (Clerck) and Tegenaria atrica. An even more effective
regenerate and its sister appendage developing without teratogenic factor, giving surprising results, is alternat-
disturbance. In the course of an experiment it is also ing temperatures. The experimental use of this factor
possible to take measurements of the regenerated induced the development of anomalies in nearly all
fragment of the leg by defining accurately the place of metameres in T. atrica (Jacun´ski, 1984, 2002;
amputation. Moreover, the presence on the leg joints of Jacun´ski et al., 2004; Jacun´ski & Templin, 2003).
characteristic external structures of cuticular origin, One of the morphological anomalies induced by
suchasspines,setaeandclaws,makesiteasiertoassess exposure of T. atrica embryos to alternating tempera-
the regenerative potential and all departures from tures is polymely, which consists of the development on
normality. It is then possible to trace the characteristic the germ band of accessory metameres, either entire or
succession of joint development in the course of epi- as halves (right or left). This changes the overall meta-
morphosis and to establish the successive regeneration mery of the prosoma and results in the development of
phases. Based on these properties of the appendages, accessory appendages, i.e. appendages which are absent
Vachon (1967) distinguished four stages in the develop- in normal ontogenic development. In the internal
ment of regenerates after traumatic epimorphosis in structure of polymelic individuals an increase in the
Coelotesterrestris(Wider)(Amaurobiidae),correspond- volumeofthenervousmassandchangesinmusculature
ing to four successive stages of their ontogenetic devel- can be observed (Jacun´ski et al., 2002). Complex
opment.AccordingtoVachon(1967)theappearanceof anomalies are another kind of anomaly which may
a certain type of regenerate (embryonal, prelarval, develop under the same experimental conditions. Their
larval, nymphal) depended directly on the time of characteristic feature is the overlapping of at least two
amputation.Thoroughstudiesofeachregeneratedjoint different deformities of appendages. Either type of
made Vachon adopt the hypothesis that the regenerates monstrosity can cause high mortality among spider
were not homogeneous, since in Coelotes terrestris they populations, which has been confirmed by researchers’
consisted of joints of different ages, the most distal reports. It therefore seems important to find out what
ones being the oldest. Similar results were obtained by kind of mechanism has been developed to protect
Mikulska et al. (1975) and Jacun´ski et al. (1994) while individualswithalltypesofstructuralanomaliesagainst
348 EffectsofappendageamputationinTegenaria
elimination from the natural environment, particularly appendages as in the experimental individuals. All the
considering that information concerning this problem is experimental individuals were photographed in each
onlyfragmentary(Mikulska&Jacun´ski,1977;Jacun´ski stage of the experiment. Moreover, histological sections
& Napiórkowska, 2000). Epimorphosis in such cases is weremadeoftheexperimentalindividuals,inwhichthe
the subject of the present study. structure and architectonics of internal organs were
analysed, in particular the overall structure, arrange-
mentandconditionofthenervoussystem.Thematerial
Material and methods
was fixed in Bouin’s solution made up according
Studiesofepimorphosisofpolymelicwalkingappend- to Zawistowski’s (1986) recipe. In order to facilitate
ages and of parts of so-called complex anomalies of penetration of the fixative the redundant appendages
appendages were carried out on Tegenaria atrica. The andtheopisthosomawerecutoff,thenthepreparations
particular developmental stages of this spider species with the fixative were put into a vacuum chamber for
have been defined according to the nomenclature 2h. They were put into the chamber again while they
adopted by Vachon (1957). were saturated with a mixture of xylene and paraffin
The experiments consisted of two stages. Before the with a melting temperature of 52(C. The paraffin cubes
first stage, whose objective was to obtain individuals with preparations were sliced 6(cid:1)m thick and after
with polymely and with complex anomalies of append- appropriate histological procedures stained with
ages,sexuallymatureindividualswerecollectedfromthe Delafield haematoxylin and eosin and mounted in
natural environment. The spiders successively obtained euparal.
intheyears1996–2002werekeptinthelaboratoryunder
conditions optimal for the species, i.e. at a temperature
Results
of 21–23(C and relative humidity of c.70%. They were
fed larvae of Tenebrio molitor (L.) and Acheta domesti- Ineightyearsofstudiesoftheepimorphicpotentiality
cus (L.) twice a week. After a short adaptation period of accessory walking appendages and of walking legs
each mature female was kept with different males, forming part of a complex deformity in T. atrica,
several hours with each, to avoid losses resulting from c.15,000 embryos were exposed to alternating
insufficient fertilisation. When oviposition started, each temperatures.
clutchwasexposedalternatelytotemperaturesof14and The death rate among the embryos in these
32(C. The temperature was changed every 12 hours for experiments was considerable (c.20%). Among the
10 days, i.e. from the moment of oviposition until the larvae which emerged from the egg membranes, 1348
first metameres of the prosoma appeared on the germ individuals were found with nearly all the monstrosities
band. Then the developing embryos were kept at 23(C foundsofarinT.atrica.Mostdeformitiesconcernedthe
until the egg chorion and the prelarval membrane were prosoma and the structure and number of the feeding
cast off. and walking appendages (c.93%). Polymelic monsters
For the second stage of the experiments, individuals accounted for only 3.75%, while individuals with more
withpolymelyandwithcomplexdeformitiesofappend- complexlegdeformitiesoccurredevenmoresporadically
ages were selected from the teratological material. Two (1.44%).
days after they shed the prelarval membrane, the
selected monsters had thin steelon thread ligatures put
Amputation of accessory walking appendages
on their polymelic walking legs and on walking legs
forming part of a more structurally complex appendage Disturbances in the prosoma associated with an
anomaly.Theligatureloopwasplacedatthemid-length increased number of appendages occurred in 47 larvae,
ofthefemur.Inthecaseofpolymelytheexperimentwas 32 of which had accessory walking appendages.
extended by putting a ligature at the place of autotomy Accessory feeding appendages appeared in only 15
between the coxa and the trochanter in other individ- individuals.
uals. The amputation ligature caused breakage in the A total of 28 larvae were selected for studies of the
continuity of the integument as well as of the muscles epimorphosis of polymelic walking legs. The remaining
and nerves running in the appendages. In this way the four cases of polymely were used as controls. The
haemocoel was also sealed, which made it possible for polymely in all these individuals was single polymely,
the spider to throw off the dead part of the appendage which consisted of the development of one accessory
during the next moult. The operated individuals were appendage.Theaccessorylegsofthelarvaeweresimilar
then placed separately in Petri dishes, where they were in their length and seven-joint structure to normal
kept through all successive postembryonal stages until walking legs. In most cases, however, their coxae were
the completion of the observations. displaced slightly toward the dorsal or ventral side
Throughouttheexperimentstheexperimentalindivid- (Fig. 1A); less frequently they lay in a line with the
uals were regularly supplied with drinking water and remainingwalkinglegsoftheprosoma.Inthelattercase
food. At first the food consisted of newly laid spider thechoiceofthecorrectappendageforamputationwas
eggs, then small Tribolium sp. and Tenebrio molitor (L.) made after studying the arrangement of mid-gut caeca.
larvae. At the same time, under similar experimental As is known (Jacun´ski, 1971, 1984), one such caecum
conditions, a control culture was maintained consisting reaches the base of each normal walking appendage.
ofindividualswiththesamedeformitiesoftheprosomal Polymely,ontheotherhand,isadeformityinwhichthe
T.Napiórkowska,L.Jacun´ski&J.Templin 349
volume of the suboesophageal part of the nervous
system is enlarged by accessory neuromeres (Fig. 1B),
but no caecum extends toward the accessory appendage
(Fig. 2A: 5). So far only one case has been described of
a larva in which an increase in the number of append-
ageswasassociatedwithacorrespondingincreaseinthe
number of mid-gut caeca (Jacun´ski et al., 2002).
Twenty polymelic larvae had ligatures put at the
mid-lengthofthefemur.Afteramputationatthenymph
I stage (Vachon stage IV), all the experimental individ-
uals retained only a fragment of the appendage, with a
scar at the place of amputation. The central part of the
usually flat or slightly bulging surface of the regenera-
tion scar was generally darker than the more peripheral
part,whichmightbeevidenceofmoreintensecuticular-
isation. However, no normal regeneration of the ampu-
tated parts was observed, nor did the missing joints
appearafterlatermoults.Consequently,throughoutthe
experiment, along with four pairs of normally devel-
oped, fully functional walking appendages there was a
short, immobile stump of the accessory appendage.
Before the completion of the experiment, i.e. until the
nymph V stage (after five post-larval moults), no
changeswereobservedinthemorphologicalstructureof
these parts of the polymelic appendages.
Fig.2: APolymeliclarvaofTegenariaatrica(dorsalview);BNymph
IIofTegenariaatricawithfourpairsofwalkinglegsandcoxal
joint of accessory leg (ventral view). Abbreviations:
1–4=normal walking legs, 5=accessory walking leg,
a–d=caecaofmid-gut.
In view of the fact that amputation of the accessory
appendages at mid-length of the femora did not lead to
epimorphic regeneration, the experiment was extended
byamputatingtheappendagesattheplaceofautotomy
between the coxa and trochanter. This amputation was
carried out in eight other polymelic individuals at the
larval stage. The effect was the same as in the preceding
variantoftheexperiment,i.e.noregenerationtookplace
(Fig. 2B).
Observations of individuals in the control sample
showed that in further ontogeny the polymelic append-
ages did not develop properly. Their growth rate was
muchslowerthanthatoftheremainingwalkingappend-
ages. At the nymph I stage the accessory appendages
were c.82% of the length of the remaining, normally
developing walking appendages, while at the nymph II
stage(aftertwopost-larvalmoults)thatproportionwas
only75%.Whilenormalappendageswereequippedwith
large pectinate claws at the nymph I stage, they did not
appear on the accessory appendages until the nymph II
stage. The accessory appendages also differed from the
normal ones in that they did not participate in the
spiders’ locomotion. In one individual of the control
Fig.1: ALarvaofTegenariaatricawithaccessorywalkingappendage group the accessory appendage was autotomised at the
displacedtoventralsideofprosoma(ventralview);BLongi- first nymphal moult. Also in that case no regeneration
tudinalsectionthroughprosomaandcentralpartofnervous was observed before the completion of the experiment.
system of Tegenaria atrica with accessory walking leg.
Thedeathrateinthisseriesofexperimentswasc.21%
Abbreviations: a=brain, b=suboesophageal part of nervous
(six individuals). The accessory appendage of one of
system, 1=ganglion of chelicera, 2=ganglion of pedipalp,
3–7=gangliaofwalkinglegs. the larvae was injured in the course of the ligature
350 EffectsofappendageamputationinTegenaria
procedure, and this caused excessive loss of haemo- At the nymph I stage well-scabbed scars were
lymph. For the remaining five spiders the critical time observed on the amputation surface. As in individuals
was the first post-larval moult. withanaccessorywalkingleg,thescarswereusuallyflat;
inonlyonecasewasthereacentralprotuberanceonthe
Amputation of fragments of appendages in complex bulging surface. At the nymph II stage (after two
anomalies post-larval moults) in cases of complex anomalies no
structural changes were observed at the place where
Complex anomalies consisted of the simultaneous
after amputation of a leg fragment the first regenerate
occurrenceinoneindividualoftwoormoredeformities,
usually appears (Fig. 3C). Also no regeneration was
such as schistomely (bifurcation of appendage), hetero-
observed at the nymph III stage (Fig. 3D) or in the two
symely (accretion of legs lying on one side of the body),
following developmental stages. Before the completion
polymely(increaseinnumberoflegs),oligomely(reduc-
of the experiment the only change observed was an
tion of number of legs) and symely (accretion of legs
elongation of the stumps, proportional to that of
lying on opposite sides of the prosoma). In the whole
the other walking appendages. All spiders lacking a
experimental period 18 larvae with complex appendage
fragment of leg moved adroitly about the web.
anomalies were obtained. The appendages involved in
Out of the five operated individuals one died as a
the anomalies were either both the walking and feeding resultofhaemolymphlosswhilethrowingoffthecuticle
appendages or only the walking legs while the feeding
in the first post-larval moult. The remaining four
appendages remained unchanged in number and in
reached the nymph V stage.
morphological structure. Only five individuals (c.28%)
were selected for studies of epimorphic potentiality. In
Discussion
all these larvae the coxal joints of the pedipalpi were
accreted with the coxae of the first walking legs, whose Theexperimentalstudyoftheepimorphicpotentialof
more distal parts were bifurcate (Fig. 3A). The remain- polymelic walking appendages and of those forming
ing cases of complex anomalies were excluded from the parts of so-called complex deformities of appendages in
experiment because of their non-recurrence. T. atrica consisted of two parts. The object of the first
The ligatures were applied on the second day after stage was to induce the above deformities by exposing
hatching.Amputationwascarriedoutatthemid-length developingembryostoalternatingtemperatures(14and
ofthefemoraofthosewalkinglegswhichshowedsingle 32(C).Thatwasfollowedbythesecondstageofstudies
schistomely in their distal parts (Fig. 3B). directly concerning the regeneration process.
Fig.3: AShallowheterosymelyofpedipalpandschistomelicwalkingleginTegenariaatricalarva,ventralview(a=accretedcoxae,b=bifurcate
walkingleg);BLarvaofTegenariaatricawithcomplexanomalyofappendages,withligatureonschistomelicwalkingleg(dorsalview);
CNymphIIwithoutregenerateofpartoftheappendagecomplex(dorsalview);DIndividualwithoutregenerateofpartoftheappendage
complexatnymphIIIstage(dorsalview).
T.Napiórkowska,L.Jacun´ski&J.Templin 351
Before the observation of changes involved in the The above statements, however, do not apply to the
regeneration process, amputation was carried out by appendageswhichindisturbedembryogenycandevelop
means of steelon thread ligatures. Tightening the on the petiolus. It is known that during embryonic
ligaturebrokethecontinuityofthetissues,andthepart development appendage buds can develop at that place
of the leg distal to the ligature was subject to necrosis on the opisthosoma, but in normal embryogeny they
induced by cutting off the haemolymph supply. During soon disappear (Jacun´ski, 1984). However, under the
this time the wound was cicatrising and being influence of teratogenic factors these buds continue
coated with a darker, and therefore more intensely developing to form jointed appendages. After their
cuticularised, integument. amputation a normal regeneration process has been
In the experiment with polymelic individuals whose observed,sometimesrecurringseveraltimesandleading
accessory leg was amputated at the mid-length of the tofullreconstruction(Jacun´ski&Templin,1991).Itcan
femur, no normal jointed external regenerates were beassumedthatthecapabilityforepimorphosisofsuch
found before the completion of observations, i.e. until legsispossiblesince,unliketheaccessoryappendagesof
the nymph V stage. Since no regenerates developed at theprosoma,theyhaveareferencetoontogeny.Similar
the place of amputation, eight other larvae obtained epimorphic potential is found in the spinnerets, which
from teratological material were operated on at the develop from appendage buds on the opisothosomal
pointofautotomybetweenthecoxaandtrochanter.The metameres (Bonnet, 1930; Ivanov, 1965).
aim of that change in research method was to find out Also, no epimorphic regenerates were observed after
whether amputation at that place, specific for the amputation of bifurcate appendage fragments in com-
epimorphosis of each appendage (Bauer, 1972) would plex anomalies. Until the nymph V stage only well
initiate the process of regeneration of the amputated scabbed post-amputation scars could be seen at the
joints. The result, however, was also negative. In this place of amputation, which may be evidence of a
case, too, the wounds were only scabbed. This process considerable narrowing of the spectrum of the effect of
can be regarded as the initial stage of the regeneration morphogenetic mechanisms. A different result was
processinarthropods,precedingthedevelopmentofthe obtainedafterautotomyofanappendagecomplexinT.
lost part of the appendage. In the above experiments it atricabyJacun´ski&Napiórkowska(2000).Afteritwas
therefore represented the first and last noticeable effect torn off at the point of autotomy in the course of the
of amputation, protecting the spider against haemo- third nymphal moult, in the following developmental
lymph loss. Evidence of the importance of this process stage there appeared a short regenerate of the larval
may be provided by the fact that the cuticle layer type,whichshowednotraceofearlierdeformity.More-
forming over the place of amputation was thicker than over, in the nymph VI stage it reached the same size as
normal.Sincenoexternalregenerateswerefound,itcan the well-developed corresponding appendage on the
be inferred that accessory appendages, which do not opposite side of the prosoma. Its further autotomy,
occur in normal ontogeny, have limited regeneration whichtookplaceseveraldaysafterthemoultfromstage
potentialities. Their development potential in further VI to stage VII, induced renewed activation of epi-
postembryogeny is also limited, evidence of which was morphic mechanisms, the result of which was the devel-
found in the observations on the control individuals. opment of another regenerate of the larval type in stage
The obvious reason for this is that the development of VII. That regenerate was almost immediately subject to
oneormoreaccessoryappendagesconsiderablydisturbs autotomy,andthesamehappenedafterthefourfollow-
the overall structure of the prosoma, thus handicapping ing moults. These newly reappearing short regenerates
thebasicvitalactivities,suchaslocomotionandobtain- were torn off. It can therefore be assumed that in some
ing food. To some extent it would also reduce the cases appendages affected by complex anomalies can
potential for reaching sexual maturity and procreation. undergo epimorphosis, although the regenerates do not
Thebestsolutionoftheproblemwouldthereforebethe always reach their final shape. Sometimes the effect of
elimination (autotomy) of the superfluous legs with no the ballast they constitute for the animal becomes too
potential for their being reconstructed. That develop- great and they are removed. The question remains, why
mental strategy would seem to be an important in only one particular case did an external regenerate
evolutionary achievement for arthropods. develop?Itmayhavesomeconnectionwiththeparticu-
The above experiments are in line with the case lar type of complex anomaly. In the study quoted
described earlier by Jacun´ski et al. (2002) of a spider in above the anomaly concerned only walking appendages
which autotomy of an accessory walking appendage (simultaneously polymely, heterosymely and schisto-
occurred in the course of nymphal ecdysis. In that mely), while in the experiment described in the present
particular case, likewise, no changes were observed paper the appendages concerned were different both in
which provided evidence of epimorphic processes structure and in function, namely the pedipalp and the
leading to the reconstruction of the cast-off fragment firstwalkingappendage.Thatmayhavebeenthebarrier
of the polymelic appendage. It can therefore be not allowing a full regeneration process.
inferredthattheaccessoryleg,despiteitswell-developed The above experiment has demonstrated that
innervation, shown in detailed histological studies polymely and other more complicated deformities of
(Fig.1B),isnotsubjecttothesamedevelopmentallaws appendagescauseareductionorcompletelossofpoten-
as a normally developed appendage (Jacun´ski et al., tial for their regeneration. There is, however, no doubt
1994). thatlegregenerationisineveryrespectaveryimportant,
352 EffectsofappendageamputationinTegenaria
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