The reproductive ecology of Euscorpius flavicaudis in England

6 Pages·1993·1.8 MB·English

by  T G Benton

M
THEREPRODUCTIVE ECOLOGY OFEUSCORPIUSFLAVICAUDIS ENGLAND
T.G. BENTON
Benton, T.G. 1993 1111: The reproductive ecology ofEuscorpiusflavicaudis in England.
MemoirsoftheQueenslandMuseumtt(2): 455-460. Brisbane. ISSN 13079-8835.
The reproductive ecology ofthe scorpion Euscorpiusflavicaudis was studied both in the
fieldin England(atacolonydatingback 120yrs),andundersemi-naturalconditionsin the
laboratory. Before the mating season males become vagrant to search for females. On
encounteringapregnantfemaleoronewithyoung,inher 'burrow',ihemalemaymate-guard
liei until herperiod ofmaternal care ends and she becomes receptive to him. Large males
have a higher mating success than small males. Two instars of adult males exist in this
population of scorpions: large 7ih instars and small 6th instars. and the reasons for this
appnrently paradoxical situation are explored. QEu.\<-y/rpius, matc-guurding, mating, life-
ktSWlv
T.G. Benton, Department ifZntdogy, University ofCambridge, Dawning St.. Cuwhr'tdgt.,
CB23EJ, UnitedKingdom; presentaddress: SchoolofEnvironmentalSciences. University
ofEastAnglia, Norwich, NR4 7TJ, UnitedKingdom; 7December, J992.
Evolutionary andbehaviouralecologyarerela- associated with buildings (Wanless, 1977).
tively young disciplines; and have to date con- Colonies have been reported from several loca-
centrated on using the more 'familiar' animalsas tions in England, but only one, at Sheemess
subjects: birds, mammals and insects. Thesedis- Docks, Kent (51°26'N, 0°45,E) has lasted munv
ciplines have largely passed arachnids by. In- yearsandisofconsiderable size.Thefirstrecord
creasingly, however, we are beginning to realise OfscorpionsatSheemessisalabelonaspecimen
the utilityofarachnidsas model animals in help- ofEuscorpiusflavicaudis in the Natural History
ingto elucidate general evolutionary principles. Museum, London: Taken in Sheemess Dock-
Although therehas been considerable increase yard, 1870, J.J. Walker' (P.D. Hillyard, in lit.).
in behavioural ecological interest in spiders in
recent years, scorpions have been largely ig- METHODS
nored. This is perhaps because they are difficult
animals with which to work - long-lived, inac- FieldObservations
tive, elusive and nocturnal. This paper outlines At Sheemess Docks, most present buildings
some ofthemain findings ofa study ofscorpion and the perimeter wall date from 1823 (Benton,
reproductive ecology. It is unfortunately incom- 1992a). Scorpions arc common in areas little
plete: posingmore questions than itsolves; bill, 1 frequentedbypeople;andarcespeciallycommon
hope that it illustrates the fact that, as in so many livingintheperimeterwall.Thisoldwallisabout
areas of their biology, scorpions arc 4m high and 66cm thick. It shows the effects of
idiosyncratic,fascinatingandmorecomplexthan time, with the mortar between the bricks crum-
they may first appear. This study combines the blingaway,creating cracks' whichthescorp
power ofcontrolled laboratory experiments and readily inhabit.Mystudy areawasa 104m length
the ease of laboratory observations with ihe of perimeter wall (bounding ornamental and
reality ofwhat is observedinthe field, and, by so vegetable gardens). The field study was OOfl
doing,forthe firsttimetheeventssurroundingthe ducted from January I9S8 to July 1989, during
courtship of a scorpion are explored and placed which 92 visits were made to Sheemess Docks
in an ecological context. (totaling 500 hours of observations). Scorp
wereobserved usinga portable ultra-violet light.
THE STUDY ANIMAL Benton (1992a) details field methods
Euscorpius flavicaudis (de Geer), common Laboratory Observations
throughout southern Europe (Birul;i. 19)7), also To allow more complete observations and ev
occurs in England, most probably ;t> a icsuit of perimentation a laboratory colony ofEuscorpius
introductions This species is a successful was set up,modelledon the habitat at Sheemess.
colonising species (Fage, 1928; Wanless,. 1977; This consisted of a plywood wall (2.44m x
Lourcnco & Vachon, 1981) and is often found 5.79m). coveredinsandpaper,with 144slots(2.5
4*i MEMOIRSOFTHEQUEENSLANDMUSEUM
,i 5,km) cut into the face. Into these slots were seen. Thenumbersbuildupduringthespringand
filled artificial "cracks* 12 cm long. These were peak in late summer (Benton, 1992a) before
opentothewall andclosedatthefarend. A layer decreasingagain to winterlevels. As these scor-
ofsoilwasplacedatIhebaseofthewalI.This soil pions live forseveral years (Benton. 1991b) this
wasperiodicallydampedtomimicrain, andeach pattern reflects varying patterns of behaviour,
weekwoodliec(thescorpion'snaturalfood)were ratherthangrossmortality andnatality. Ft* rims'
reJcased onto it. This colony was kepi under a oftheyear, mostscorpionsseenareintheircrack
natural photopcriod.andas nearnatural tempera- (for NovembertoJune only 8± 11% ofall scor-
ture and humidity as possible. Observationsand pionsobservedareoutoftheircracks).Hov.
±9%
experiments were conducted at night, when the in summer, on average, 24 of scorpions
wall was illuminated by lamps fitted with deep- observed were on the wall surface. Adult males
redfilters(invisibletoscorpions:Machan, 1968). makeupmostsurface-activeanimals 3-4x more
Unlessbeingusedinanexperiment,thescorpions males are seen on the wall surface than adult
(collected at Sbecrncss) were allowed to move females overthesummer(Figs la, b)
freely around the wall Benton (1991*0 details The number of females giving birth or with
colony setup. young peaks when female activity on (he waJl
surface (Fig. la) is least. Females with young
EXPI I i Mi Hi' 'lis remain deep within their cracks, and were: never
In this study of male contest behaviour for observedtoventure ontothewallsurface Indeed,
females duringthe mating season, 1 1 maleswere females in the last singes of pregnancy also ap-
used On the artificial wall40x40cmenclosures peared to show a marked reduction in activity.
were made around a single crack A female car- Most matings at Shccrness (Fig. lb) are just
ryingyoung wasplacedinthiscrack,and lateran after the number of females with young peaks
experimental male was added. Thirty minutes (Fig. 1a). Knownfemaleswithyoung were found
alter this male had encountered and entered the to be unreceptive to males until 2±1.2 days
crackasecondmalewasadded.Afterencounter- (n=l2) after the juveniles had moulted and
ing the crack the second male would attempt to climbedoffherdorsum (Benton, 1992b*
enter. The males would then meet, assess each
other and fight. This procedure was then imme- About 3 weeks otter male surface-activity
diatelyrepeated.The two replicates constituted a begins, the number of matings observed peaks
contest' (and ui all cases the resultswere unam- (Fig. lb). Only atthistimecan malesandfen
biguous,and identical foreachreplicate). Intotal be found together in the same crack. These
periods ofcohabitation averaged 10±9.9 nights
'1o1w0nceorn'teasgtasinwsetreevceornyduocttheedr (mwailteh eaaschinmtrauldeer)a.s (range I-30; n=19: data from field). Cohabiting
Contest order was randomly selected. Other occurred only prior to mating, and whilst the
methods aredetailedin Benton(1992b).andscor- femalewaseithercarrying young, orinlate preg-
pion mensuration in Benton(1991bi nancy (Benton, 1992b). Males were aSSOCi
sometimes with females living in shallow cracks
RESULTS 1 it=3)i in which case the males spent the day in a
deep crack nearby and 'commuted* to the
female's crack to spend the night sitting at the
Background entrance. The identity of the male mating with a
Like mo^i scorpions, &, Jluviawdis is noctur- specific female was known for 15 cases of
nal. During the day andoverthe winter, they are cohabitation: in 14 the male had been recently
not visible as they have retreated to the back of ci"habiting (P<0.00:o with that female. Females
their cracks in the wall. At night, depending on ofthis species do not appearto assess males, and
the season, most scorpions evident are at the will mate with any male present when they be-
entrance to their cracks where they remain im- come receptive (Benton, 1992b). Ifa male's en-
mobile, with their claws outstretched and open, counter rale with females is low, and a female's
The most common prey items are isopods {Por- tecCptivity ispredictable, then a maleencounter-
i vUiosaiher){hA%)andthenCOnspOCffics( I _ ing a soon-to-be receptive female may do better
(Benton. l9Wa) waiting for her to become receptive, rather than
leaving her and risking trying to find a female
Seasons nearerreceptivity(Grafenand Ridley. 1983);and
Scorpion activity at Shccrncss is highly this seems to be the case with these scoipions
seasonal. Overthewintervery few(ifany)canbe (Benton, 1992b). This behaviourcanalso benefit
1
REPRODUCTIVEECOLOGY OFELSOORPtL'S FLAWCAUDIS 457
To investigate male mate-guarding contests
15 1 Fig 1a 110contestswerestagedbetween 1 1 males(each
male as 'owner' against each of the others as
'intruder"). The proportion ofcontests won cor-
related very strongly with measures ofscorpions
size, and most strongly with pedipalpal claw
length frs=0.97tP<0.001). This is to be expected
as£flaxicaiidis uses its claws as its main offen-
sive weapon. In 80% of contests, the larger-
clawedmale won: when thesrnallcr-clawedmale-
won (2(r%), it was the "owner1 in most (91%)
contests. Both relative claw-size and ownership
r -,.,-, •;i"in 4ft1 status had highly significant effects on contest
Days outcome (two-way ANOVA, size: F=68.5; di
15-
FTfl 1b J,36; P<ll.C)niJl; status: F=42.7; df |,36j
P<0.000l): iarge-clawedmalesusuallywoncon-
tests, but if contestants were closely matched in
10-J size then ownership status decided the outcome
(giving an advantage equivalent to about 11%
longerclaws).
Size and Sexual Advantage:
In the laboratory, males differed in reproduc-
tivesuccess:somemalesmatedtwice,someone*:
4C0 and some not at all. Larger males mated more
often than small males (Fig. 2). This size ad-
vantage is for two reasons. Firstly, as described
PIG. 1 ReproductiveseasonofKuscorpiusjlavicaiidis above, larger males are better competitors for
in England, 1988. (a) Seasonality of adult female female-occupiedcracks. Secondly,about40
surface-activityand no.ofbirths. Femalesurface-ac- matings are not preceded by mate-guarding.
tivity is smoothed over two weeks: nightly count These fall into three broad categories: non-preg-
shownasaverageofpreceedingandfollowingweek's nant females at the start ofsummer, females n-ot
counts.No.ofbirths(foreachhalf-month)estimated found by males before their maternal care has
from no. offemalesgiving maternal care, and dateat endedand(mostrarely)femaleswhohave mated
fwahciec-hacttihvisiteynd(esdm,oo(tbh)eSdeaosvoenraltiwtoy-owfeeakdsu)l,t maanldehsaulrf-- already (this is possibleasa spermatocleutrum is
monthly count of no. of matings (observed no. of not secreted in this species). Large males obtain
matings plus no. of spermatophorcs found). Data morematingsfromall threecategoriesthansmall
originally, inpart, in Benton 1992b. males. This is because, for each category of
mating, females are initially unwilling to o
the femalesfortworeasons. Firstly,itensuresthat When a female is mate-guarded prior to her
they are mated. Secondly, a major advantage of receptivity, she encounters the male frequently,
and upon becoming receptive begins courting
maternal careinscorpionsis topreventpredation
ofthejuveniles(Benton, 1991a),sohavingamale without aggression. Conversely, when a male
atthefrontofthecrackpreventsentrancebyother encountersanon-pregnantfemale,oronewithout
scorpions which may aid this role. young he immediately attempts to court. The
male grabs (or attempts to grab) the female's
In all cases ofcohabitation, the male stations claws and stings her (Benton, 1990). Indeed, the
himselfneartheentrance, withthefemalebehind
start of a courtship {without mate-guarding) is
him- Males attempting to enter the crack en- indistinguishable from a cannibalistic attack.
counterthe currently cohabiting males, andeach Large males are better at mating with these un-
triestograspthe other'sclaws. Withina veryfew willing femalesas, unusuallyforscorpions,large
seconds one male retreats and tlees from the malescan be largerthan females. In this specie.
crack. Males therefore tight for 'possession' ofa and others (Polis, 1980), size (especially clav.
crack occupied by a female in the period before size) is a good predictor of the outcome ofcan-
shebecomes receptive. nibalisticcontests.Atthestartofcourtship,males
458 MEMOIRSOFTHEQUEENSLANDMUSEUM
10
triehobothria
lmm
-0.5 0.5 1.0 2.C
Mating Success
FIG. 2. Relationship between size (claw-length) and
mating success in laboratory males free on wall sur-
face(mean±SD). Differencebetween groupsissig-
nificant(Kruskal-Wallis,H=l1.4,P=0.003).
sting females, and larger males can eat adult
females (and often do: 10 cases observed in the
laboratory), therefore, large males essentially
give females the choice ofbeing cannibalised or
lmm
accepting courtship. Small males obtain fewer
matings as they have a smaller (or nonexistant)
size-advantage over females (Fig. 3) and there-
fore are more likely to flee from those females
whoare not immediately willing to court.
SizeDimorphism
Sexually matureadult males are recognisedby FIG. 3. Clawsoftwoadult 86 (a, b) andoneadult 9
the secondary sexual characteristic ofa notch in (c)samescale. Notesecondarysexualcharacteristic:
the pedipalpal fingers (Fig. 3). Adult males can notch in fingers.
dininofctfrieecraesamebaslreaklwelhdomeleyntroiinnceasliclzyoen,wsiiatdnhedrbsotdchiylsaswiizssei,ezssep,ueccwhihatilhclahyt ibneesnormeeporstpeiddeirnssc(eo.rgp.ioVnosl,lrbautthi,sk1n98o0w;nWtaotoscocnu,r
1990) and occurs widely across the animal
largermaleshavedisproportionatelylargerclaws
(Fig. 3).Thefrequencydistributionofadultmale kingdom(Ridley, 1983).Forprecopulatorymate-
claw sizes at Sheerness was dimorphic (Fig. 4). guardingtoevolve,malesmustgainanadvantage
Thisdimorphismalsooccurswithothermeasures by staying with a female prior to her becoming
ofsize, suchasprosomalength (Benton, 1991b). receptive rather than searching for a receptive
Thisdimorphismprobalyarisesbecausethereare female. Two criteria may determine this situa-
two instars of adult male in the population at tion: firstly, ifa male can predict when a female
Sheerness: 6th and7th (seealso Benton, 1991b). is going to become receptive, and, secondly if
receptivefemalesaredifficulttofind.Theformer
DISCUSSION mayoccuriffemalesbecomereceptivefollowing
a moult (e.g. Watson, 1990), or as in the case of
Two points are noteworthy. Firstly, the these scorpions, after maternal care. The latter
reproductiveecologyofEuscorpiusflavicaudisis criterion may result from female receptivity
much more complex than previously imagined. being very limited in time (e.g., in Gammarus
Naively placing pairs of scorpions together in a female receptivity is limited to a brief period
laboratorysituationtowatchthecourtshipwould between moulting and the hardening of the
present a very misleading picture because the amphipod's exoskeleton: Grafen and Ridley,
most significant behaviours occur before actual 1983), low population densities (and so low en-
courtship. Precopulatory mate-guarding has not counterrates) orbecause ofhigh male mortality
REPRODUCTlVEECOLOGYOFEUSCORPIUSFLAVICALTMS 459
is equal. This ESS could be maintained by fre-
quency dependent selection (Benton, 1992b):
largemalesdorelativelybetterwbenrare(asthey
suffer little competition) so their frequency is
increased in the population by natural selection.
However, when large males are common their
gainsarereduced, becauseofincreasedcompeti-
tion between them, to a point where they are
offsetbythecostofdelayingmaturity. Hence, %[i
evolutionary equilibrium is reached between the
a t3> t1>8 ^8 CI3S 8 fr—t genes controlling maturation at the 6th and 7th
£ i * * 6 instars.
en
Secondly, an alternative explanation for this
Clawlengthf/nm) paradoxisthattheremaybephenotypicplasticity
A
FIG 4. Distribution ofelaw-si7.es in adult 63 is sig- inthe maturation stage gene that canproduce
nificantly non-normal. Filled bars arc observed dis- a variety of phenotypes depending on the
tribution; stippled bars are expected normal vironmentissaidtoexhibit phenotypic plasticity
distribution given mean and standard deviation of (Lessels, 1991). The 'optimal* time at which to
data.(x2=2U.P<0.005>. mature may depend on factors such as food
availability, and thus growth rate (Stearns ai»d
during mate-searching (Vollrath, 1980). The Koella, 1986). For example, if food is plentiful,
periodoffemalereceptivity isreducedwhere the and an individual is large forits cohort it maybe
pdteitiit]/ Ofa male is ensured by being ihe first besttomatureearly. Conversely, ifan individual
mule to mate with a female (so called first-male issmallforitscohortthenitmaybebettertodelay
spermpriority),whichmaybecommoninarach- maturity until more food is encountered. This
nids(e.g.Vollrath, 1980;Watson, 1990).Avirgin seems to be the case in manv spiders (e.g.,
female is far more valuable to a male than one Deevey, 1947: Vollrath. 1980). this subject will
which is already mated. Thus, Euscorpius be discussed further elsewhere (Benton, in
fhsvicaudis, first-male sperm-prinrity and low prepjration),
population densities, coupled with the female's
receptivity being predictable, may make it more LITERATURECITED
profitable for a male encountering a female
engagedinmaternal carelomate-guardherrather BENTON.T.G. 1990. 'The behaviour and ecology of
than risk searching for another female nearer scorpions.'' (UnpublishedPh.D. thesis.University
receptivity ofCambridge)
1991a. Reproduction and parental care in the soot-
Secondly, there seems to be a paradox. Adult pion.Euscorj)iu.\rflaxicuudis.Behaviour 1 17:20-
males exist astwo instars in the population. This 28.
itself is not a novel finding (sec Francke and 1991b. The lilt* history Ol littscorpiuxJlav'icaudix
es, 1982)' M IS surprising that any males ma- (Scorpioncs.Chaetidac).JournalofAraehnology
ture at the smaller instar since the smaller males 19: 105-110.
seem to be at such a disadvantage in obtaining 1992a. Determinants of male mating success in a
mates. Natural selectionwould quicklyeliminate scorpion. Animal Behaviour43: 125-135
any tendency tomatureatadisadvantageoussize. !992b. The ecology ofEuscorpiusflavicat-u
England.Journal ofZoology, London 226:331-
The paradox suggests two explanations. First, 368.
large males may have an advantage only in a BIRULA, A.A.B. 1917. 'Scorpions: Fauna ofRussia
matingseason. As large maleshavemoreinstars, and adjacentcountries; Arachnoidea, Volume 1:
tiiL> probably take longer to mature. Although Scorpioncs.' (Petrograd: translated from theRus-
males mate more in the short-term, the younger sianbytheIsraeliProgrammeofScientificTrans-
they mature presumably the more seasons in lation,Jerusalem, 1965).
which to find mates. Perhaps there is a mixed DEEVEY, G.B. 1949. The developmental history of
Latrodecius nutcTans (Fabr.) at different rates of
evolutionarilystablestrategy CESS) such that the feeding. American Midland Naturalist 42: 189-
short-term gains enjoyed by 'large males* are 219.
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inwhichtomate,sothat,onaverage, the lifetime guarding. Journal of Theoretical Biology 102
reproductivesuccessofMarge* and 'small* males
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et 1'acclimation en France de V "Euscorpius thedemography and activity in a natural popula-
flavicaudis"(DeGeer).AssociationFrancaispour tionofdesertscorpions.BehaviouralEcologyand
1'avancement des sciences, La Rochelle 1928: Sociobiology7: 25-35.
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oAfraCcehnntorluorgoyid9e:s22g3ra-c2i3l9i.s (Latreille). Journal of STEARNS,S.C.&KOELLA,J.C. 1986.Theevolution
LOURENCO, W.R. & VACHON, M. 1981. Comple- of phenotypic plasticity in life-history traits:
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brasiliensis(Mello-Leitao, 1931) (=Teuthraustes maturity. Evolution40: 893-913.
brasiliensis Mello-Leitao, 1931), synonyme d'- VOLLRATH,F. 1980.Malebodysizeandfitnessinthe
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