Table Of ContentBull.Br.arachnol.Soc.(2002)12(5),237–241 237
Changes in brain monoamines associated with et al., 1993). An increase in 5-HT levels in the SEG has
agonistic interactions between males of Eremobates been implicated in the onset of flight behaviour in some
marathoni (Arachnida, Solifugae, Eremobatidae) beetles (Guerra et al., 1991). Lobsters winning staged
encounters(fightingbouts)withconspecificsexhibiteda
Fred Punzo ‘‘dominant’’ posture that was accompanied by higher
levels of 5-HT in various regions of the CNS when
DepartmentofBiology,
Box5F,UniversityofTampa, compared with subordinate animals (Kravitz, 1988).
Tampa,Florida33606,USA The vast majority of studies concerning neurochemi-
cal correlates of behaviour in arthropods have been
Summary conducted on insects, while other taxa have received far
lessattention(Lin&Roelofs,1992;Punzo,1985,1996).
Experiments were conducted to determine the effects of The solifugids (Arachnida, Solifugae), which have
agonisticencountersbetweenconspecificmalesonchanges
proved difficult to maintain in captivity (Punzo, 1998a),
in monoamine concentrations in the brain of the solifuge
have been virtually ignored, especially with respect to
Eremobates marathoni Muma & Brookhart. Serotonin (5-
HT) levels were significantly reduced within 30min after their physiology and neurobiology.
fighting in both dominant and subordinate animals as Solifugidsarewellknownfortheirpugnaciousbehav-
comparedwithisolatedcontrols,andthesedifferencesper- iour and voracious feeding habits (Muma, 1967; Punzo,
sisted for up to 24h. A similar decrease was found for
1998a, 2000). Both males and females exhibit a charac-
octopamine(OA).Inaddition,5-HTandOAweresignifi-
teristic ‘‘threat display’’ when they are disturbed in any
cantlylowerinsubordinatevs.dominantsolifugids.Agon-
istic interactions had no effect on the concentrations of way (Cloudsley-Thompson, 1961; Muma, 1966; Punzo,
dopamine. This is the first demonstration of the possible 1998b, c). If one encounters another solifugid and/or a
role of monoamines in communicative displays and the potential predator, the animal will typically stand its
establishmentofsocialstatusinthesearachnids.
ground, open its massive chelicerae (jaws), lift itself via
the three pairs of walking legs (legs II–IV) thereby
elevating the body, and rock its body in an alternating
Introduction
backward and forward motion. After a variable period
Over the past two decades there has been a concerted of time, the solifugid may either flee or strike at its
efforttoanalysetheroleplayedbyCNSneurotransmit- antagonist. It is not unusual for the contest to escalate,
ters (NTs), comodulators, and neurohormones in the resulting in the death of one or both combatants. Most
mediationofbehaviourinvertebrates(Eichelman,1987; malesolifugidswillexhibitthisthreatdisplayevenwhen
Summers & Greenberg, 1995; Summers et al., 1998; confronted by a conspecific female before the onset of
Punzo, 2001a). However, there have been significantly courtship.
fewer studies on neurochemical parameters associated The purpose of this study was to investigate neuro-
with behaviour in general, and agonistic interactions chemical parameters associated with agonistic interac-
specifically, in arthropods and other invertebrates. For tions between adult males of the solifuge Eremobates
example, changes in levels of brain monoamines marathoni. Specifically, I was interested in whether or
were shown to accompany a variety of ontogenetic not there were any differences in the concentrations of
shifts in behaviour in honeybee workers, including dif- monoamines (OA, DA, and 5-HT) in the SEG of
ferential discrimination between various olfactory cues dominant (winning) vs. subordinate (losing) males fol-
(Macmillan & Mercer, 1987) and the onset of nest- lowing agonistic encounters. To my knowledge, this is
guardingbehaviour(Mooreetal.,1987).Increasesinthe the first study to address neurochemical correlates of
synthesis of protocerebral biogenic amines, RNA, pro- aggression in the Solifugae.
tein, and acetylcholinesterase (AChE) have been shown
to accompany learning in crustaceans (Punzo, 1985),
insects (Lin & Roelofs, 1992; Punzo, 1996), and spiders Methods
(Punzo, 1988a).
Animals and housing
With respect to the relationship between hormones,
NTs, and the mediation of aggression and dominance Males were collected during June through August
status in arthropods, it was found that octopamine 1997 at the northern entrance to Big Bend National
turnover rates increased significantly after fighting Park (28)37*N; 102)55*W; Brewster county, Texas;
between conspecifics in the cricket Gryllus bimaculatus Chihuahuan Desert). A detailed description of the top-
(Adamo et al., 1995). Active defence of the nest against ography of this site as well as the dominant vegetation
intruders was shown to be correlated with higher con- can be found elsewhere (Punzo, 2001b). Adult male
centrations of octopamine (OA), dopamine (DA) and solifugids(Eremobatesmarathoni)wereabundantduring
serotonin (5-HT) in the supraoesophageal ganglion thisperiodandwereeasilyfoundatnightmovingabout
(SEG) (brain) of worker honeybees (Harris & on the surface between 2100–0200hCST. Solifugids
Woodring, 1992). It has been suggested that OA is part werecollectedmanuallyandweighedtothenearest0.1g
of a general arousal system which prepares insects and using a Ohaus Model 87 portable electronic balance
other arthropods for a variety of vigorous skeletomus- (Central Scientific, Chicago, IL).
cular activities, territorial defence, and helps the animal Solifugids were transported by van back to the
cope with stressful conditions (Corbet, 1991; Orchard laboratory within 72h after collection, and housed
238 BrainmonoaminesinEremobates
individually in holding cages as described elsewhere recorded as the ‘‘winner’’ (dominant animal), and the
(Punzo,1998b).Thefloorofeachcagecontainedalayer opponent that fled, the‘‘loser’’ (subordinate). Each pair
of loose sand and an artificial hollowed ‘‘log’’ in which ofcombatantswassubjectedtoonlyoneencountertrial,
they could seek shelter. They were provided with water following a protocol previously described for lizards
ad lib and fed three times per week on a mixed diet of (Summers & Greenberg, 1995). I conducted a total
crickets (Gryllus sp.), mealworm larvae (Tenebrio of 60 encounter trials, each consisting of 60 paired
molitor) and cockroaches (Periplaneta americana). They combatants.
were maintained at 22&1)C, 65% RH, and a 12:12 LD
cycle, in a Percival Model 805 environmental chamber
(Boone, IA). Animals were kept in these conditions for Neurochemical analysis of brain tissue
at least 2 weeks and then re-weighed on the day before
the initiation of encounter trials. Since previous studies Immediately following their designation as dominant
onarachnidshaveindicatedthatdifferencesinbodysize or subordinate (based on the outcome of encounter
may influence the outcome of agonistic encounters trials), paired combatants were randomly assigned to
(Punzo, 2000), only males of approximately the same one of three groups. Each group consisted of 40 solif-
size (6.1–6.4g) were used for encounter trials and sub- ugids (20 pairs). Solifugids in group 1 (G1) were anaes-
sequent neurochemical analyses. Voucher specimens thetisedwithCO thirtyminaftertheirencountertrials,
2
have been deposited in the University of Tampa and their brains (SEG) removed in a cold room as
Invertebrate Collection. describedpreviously(Punzo,1993),weighedtothenear-
est 0.1g, and frozen at "80)C for subsequent neuro-
chemical analysis. Solifugids in G2 and G3 were
Encounter trials
anaesthetised and their brains removed and frozen at
I used a rectilinear glass container (26#16#12cm), 24h and 48h, respectively, after encounter trials. This
divided in half by an opaque divider, as an encounter allowed me to determine not only what changes in
chamber to stage encounters between conspecific males monoamine concentrations, if any, might accompany
as previously described (Punzo, 1998c). The floor of the male-male aggression, but also the rapidity of the
chamber was provided with a layer of loose sand. All response,andhowlongthesechangesmightpersist.The
observations were conducted under Black lighting (Bio- brains from another group of 20 solifugids (G4) main-
Quip Inc., Model 2804, Gardena, California) behind a tained in isolation and not exposed to encounter trials
one-way mirror to minimise disturbance to the animals. were used as controls.
I used a Sony 124L tape recorder to record verbal The SEGs from dominant, subordinate and control
descriptions of each encounter. In addition, encounter solifugidswereanalysedtodeterminetheconcentrations
trials were filmed with a Panasonic MVC-F81 video of those monoamines that have been identified as NTs,
camera. neuromodulatorsorneurohormones(5-HT,OA,DA)in
Beforeeachencountertrial,onemalesolifuge(chosen arachnids (Meyer, 1991), insects (Orchard, 1982; Som-
at random) was placed at each end of the chamber, bati & Hoyle, 1984; Downer & Hiripi, 1993), and
separatedbythedivider.Atrialwasinitiatedbyremov- crustaceans (Yeh et al., 1996), using the protocol (high
ing the divider and allowing the animals to interact. performance liquid chromatography with electrical
Within a period of time ranging from 0.5–2.5min over detection; HPLC-ED, Beckman Model 47A) previously
alltrials,thecombatantsmadecontactwithoneoftheir described in detail elsewhere (Punzo, 1994). To summa-
first pair of walking legs. In solifugids, the first pair of rise, brains were removed from the head capsules as
walking legs (front legs) are elongated and used as described by Punzo & Malatesta (1988). All glandular
sensory (tactile) organs and not for ambulatory move- and fatty tissues were carefully removed from the sur-
ment (Punzo, 1998a). In a few cases (n=7), one or both face of the brain samples. Individual brains were then
ofthesolifugidswouldimmediatelyattempttofleeafter weighed to the nearest 0.01g in a Sartorius Model 54C
making initial contact with its opponent. These trials electronic analytical balance. Each brain sample was
werenotusedindataanalysis.Inallothertrials(n=60), placedina500(cid:236)lglassvial.Fifty(cid:236)lof200mMperchlo-
followinginitialcontact,bothsolifugidswouldtypically ric acid were added and the sample homogenised.
faceoneanotherandmoveoneorbothofthefrontlegs Following homogenisation, an additional 50(cid:236)l of per-
over the body of their opponent. During this sequence, chloric acid were added to each vial. Samples were then
each combatant exhibited the threat display described centrifuged at 10,000g for 3min in a Sorvall Model
above (body elevated and moved in a backward– 100A high speed centrifuge. Twenty(cid:236)l of supernatant
forwardrockingmotion,cheliceraeopened).Inalltrials, were injected directly into the HPLC column (40cm in
this behaviour would continue until the fight escalated, length,witha0.2(cid:236)porediameter)packedwithHypersil
with one or both solifugids attempting to bite the other and provided with a Hewlett-Packard 760E detector
before one of them backed away and tried to escape (0.40V). The mobile phase flow (flow rate 3000psi)
(usually by attempting to crawl up the sides of the used to elute the monoamines consisted of 20mM
chamber). A trial was considered terminated if at any sodium acetate, 12% acetonitrile, 100mM sodium dihy-
time during the encounter one of the animals backed drogen orthophosphate, 0.3mM EDTA disodium salt
away and rapidly fled from the vicinity of its opponent adjusted to pH4.2, and 2.5mM octane sulfonic acid.
(Punzo, 1998c). The solifugid that held its ground was Each sample was compared with 5-HT, DA and OA
F.Punzo 239
standards tested at the beginning of each assay run and with fighting occurred rapidly, since they were detected
retestedat30-minintervals.Monoamineconcentrations after only 30min following an agonistic encounter.
(pmol/mg brain tissue) were expressed as means&SE. AsimilarpatternwasfoundforOAlevels,whichwere
also significantly lower in subordinate vs. dominant
animalsafter30min(t=3.67,p<0.05)and24h(t=3.03,
Statistical analysis
p<0.05). However, they returned to those levels associ-
All statistical procedures followed those described by ated with isolated controls within 48h (Table 1). With
Sokal & Rohlf (1995). Comparisons between mean respect to DA, no differences were found between solif-
concentrations of monoamines for the various groups ugidsexposedtoagonisticencountersvs.controlsatany
wereconductedusingananalysisofvariance(ANOVA), time interval (p>0.5).
followed post-hoc by a Duncan’s multiple range test.
Significant differences between dominant and sub-
Discussion
ordinate males following aggressive encounters were
determined using an independent-samples t-test. Agonisticinteractionsbetweenconspecificsareknown
tobeassociatedwiththesynthesisandreleaseofspecific
NTs, comodulators, and hormones associated with the
Results
stress response in numerous vertebrate taxa (Ansell &
Following an encounter, the dominant animals con- Bradley,1973;Eichelman,1987;Summers&Greenberg,
tinued to exhibit the threat display while holding their 1995; Punzo, 2001a). Although much of the research
ground for a period of time ranging from 0.5–1.5min, initially focused on the role of hormones, such as
before assuming a normal posture (with chelicerae testosterone and adrenocorticosteroids (Sapolsky, 1986;
closed and body lowered). The subordinate animals, Greenberg & Crews, 1990), in the mediation of aggres-
whichhadbeenremovedfromthechamberimmediately sivebehaviourandsocialdominance,investigatorshave
after attempting to flee (so that aggression could not more recently turned their attention to the possible role
escalate further), typically attempted to bite the plastic of the CNS and various NTs (Summers et al., 1998;
container used in their removal. However, when they Punzo, 2001a). For example, the social status of subor-
were released onto the floor of their individual holding dinate animals is associated with an increase in the
cages, they immediately sought refuge within the arti- utilisation of 5-HT in various brain regions from fish to
ficial log. In some cases, they did not leave their refuge mammals (Sapolsky, 1986; Haney et al., 1990; Winberg
for up to 24h. et al., 1997; Summers et al., 1998). In addition, acti-
The data shown in Table 1 indicate that serotonin vation of brain catecholaminergic systems including
(5-HT) was the monoamine found in highest concen- DA, norepinephrine, and epinephrine is associated with
tration in the brains (SEG) of isolated controls of increased levels of aggression and dominance in verte-
E. marathoni, followed in decreasing order by OA and brates (Mason, 1986; Haney et al., 1990; Matter et al.,
DA (Scheffe F=3.14, p<0.01). 1998). The results of the present study indicate that
The effects of agonistic interactions between con- similar neurochemical parameters are associated with
specific males at various time intervals following aggressive behaviour in arachnids.
encounter trials are also shown in Table 1. Levels of Althoughtheprofileformonoamineconcentrationsin
5-HT after 30min were significantly reduced in solif- theSEGofE.marathoni(5-HT>OA>DA)isingeneral
ugidsthat‘‘lost’’encounters(subordinates)ascompared agreement with what little information is available on
with dominant animals (t=3.91, p<0.05) as well as with the neurochemistry of other arachnids (Meyer, 1991;
controls (t=6.78, p<0.01). This difference persisted for Punzo, 1993, 1994), it should be pointed out that
at least 24h (t=3.59, p<0.05), with levels returning to differences in monoamine profiles can vary between
normal after 48h. Changes in 5-HT levels associated different arachnid orders and between different families
within an order (Florey, 1967; Meyer, 1991; Punzo,
1988b, 1993).
Timeafterencounter The most pronounced changes in monoamine levels
Monoamine Controls 30min 24h 48h
associated with reduced aggression involved 5-HT,
Serotonin(5-HT) 54.8(6.5) occurring in subordinate males within 30min of an
Subordinate 36.1(2.1) 36.9(0.9) 56.2(2.3) agonisticencounter.Levelsof5-HTwerealsoreducedin
Dominant 46.1(1.2) 45.4(1.8) 52.5(2.6)
dominant males as compared with isolated controls. A
Octopamine 23.2(5.4)
similar reduction in OA levels was also observed in
Subordinate 10.7(0.5) 16.9(0.4) 21.7(1.4)
Dominant 17.4(0.7) 21.9(0.8) 23.8(1.8) dominant males. This is interesting in view of earlier
Dopamine 13.3(3.5) reports that OA and 5-HT often work antagonistically
Subordinate 13.9(1.1) 15.2(0.7) 13.9(0.6) (Bicker & Menzel, 1989). Thus, the act of fighting (and
Dominant 14.2(0.5) 13.6(1.1) 12.7(0.7)
thestressassociatedwithit)inmalesolifugidsresultedin
a decrease in SEG serotonin levels. This is the first
Table 1: Concentrations of various monoamines (pmol/mg) in the demonstration of an association between monoaminer-
supraoesophagealganglion(brain)ofisolatedcontrolsand
gic activity and aggression in solifugids. Changes in
subordinateanddominantmalesofEremobatesmarathoni
serotonin have been previously associated with aggres-
following agonistic encounters. Data expressed as means
(&SE).Seetextfordetails. sive behaviour in crustaceans (Kravitz, 1988; Bicker &
240 BrainmonoaminesinEremobates
Menzel, 1989; Yeh et al., 1996). The injection of 5-HT &Menzel,1989).TheinjectionofOAintofreelymoving
intolobstersandcrayfishcausedthemtoflextheirtails, lobsters elicited submissive postural responses toward
aresponseassociatedwithadisplayofdominanceinthis conspecifics (Kravitz, 1988). The application of OA
group (Yeh et al., 1996). caused engorged ticks to detach from their hosts
The present study demonstrates that lower levels of (Mason, 1986). For OA, direct comparison with verte-
aggression and dominance in solifugids are associated bratesisnotpossiblesinceOAhasnotbeenidentifiedas
withchangesinmonoaminesinthebrainthataresimilar an NT in this group.
to those that have been well established for vertebrates. In summary, significant changes in concentrations of
A variety of stimuli, including social interactions, acti- 5-HT and OA in the SEG were found to be associated
vate neuroendocrine stress mechanisms in vertebrates, with agonistic behaviour in male solifugids. It has been
which are thought to be mediated by changes in CNS well established that 5-HT is an NT involved in the
neurotransmitters brought about primarily by the acti- mediation of dominance and aggression in vertebrates,
vation of monoaminergic systems (Ansell & Bradley, and the results of this study suggest that 5-HT and OA
1973; Eichelman, 1987; Summers et al., 1998). For concentrations in the SEG are important for the estab-
example, 5-HT levels decreased significantly after oneh lishment of social status and the elicitation of com-
and one day in the brain (diencephalon and non-optic municative displays in arthropods as well. Future
lobe midbrain) of the lizard Anolis carolinensis after endeavours should assess the role of monoaminergic
losing aggressive encounters (Summers & Greenberg, systems in other species of solifugids as well as other
1995).Similarly,nochangesweredetectedforDAlevels arachnid and arthropod taxa in order to determine if
over these time intervals. However, subordinate males similar changes in monoamine profiles accompany
had significantly lower DA levels after one week as aggressive behaviour in these groups.
compared with subordinates after one h. In another
study, changes in serotonergic content and turnover
Acknowledgements
betweenindividualsofdifferentsocialstatuswerefound
in the telencephalon and diencephalon of territorial vs. I wish to thank B. Garman for consultation on
satellite males in the lizard Sceloporus jarrovi (Matter statistical procedures, T. Punzo for assistance in main-
et al., 1998). In addition, levels of 5-HT in the telen- tenance of captive animals and technical assistance, K.
cephalon and diencephalon were found to decrease Johnson for assistance in collecting solifugids in the
significantly following male-male aggression in rodents field, and P. Merrett, L. Johnson, F. Bradshaw, and
(Haneyetal.,1990)andfish(Winbergetal.,1992,1997). anonymous reviewers for comments on an earlier draft
Octopamine levels also decreased significantly in of the manuscript. A Faculty Development Grant from
males of E. marathoni following agonistic encounters. the University of Tampa made much of this work
This is in agreement with previous work indicating that possible.
OAappearstobecentraltotheelicitationoftheoverall
arousal response of arthropods (Kravitz, 1988; Corbet,
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