Trophic specialization of a newly described spider ant symbiont, Myrmecicultor chihuahuensis (Araneae: Myrmecicultoridae)

Abstract

The spider Myrmecicultor chihuahuensis Ramrez, Grismado & Ubick (Myrmecicultoridae) was described in 2019 and hypothesized to be a myrmecophile, living inside the nests of Novomessor (Myrmicinae) and perhaps also Pogonomyrmex (Myrmicinae) ants. To test the hypothesis that M. chihuahuensis are chemical mimics of their host ants, we carried out behavioral bioassays to observe interactions between the spiders and the host ants. We compared the cuticular hydrocarbon (CHC) profiles of the spiders and the ants. We discovered that this new species of spider is a myrmecophage, displaying hunting strategies similar to other myrmecophagous spiders, particularly those in the genus Zodarion Walckenaer, 1826 (Zodariidae). The CHC profile of M. chihuahuensis did not match the profile of the ants with which it associates, Novomessor albisetosus (Mayr), but ants and spider shared several compounds, potentially involved in species recognition.

Full text

2022. Journal of Arachnology 50:250–255
SHORT COMMUNICATION
Trophic specialization of a newly described spider ant symbiont,
Myrmecicultor chihuahuensis (Araneae: Myrmecicultoridae)
Paula E. Cushing
1
,Adrian Br ¨
uckner
2
,Jesse W. Rogers
3
and Norman V. Horner
4
:
1
Department of Zoology, Denver
Museum of Nature & Science, Denver, Colorado USA; E-mail: Paula.Cushing@dmns.org;
2
Division of Biology and
Biological Engineering, California Institute of Technology, Pasadena, California USA;
3
Emeritus, Department of
Chemistry, Midwestern State University, Wichita Falls, Texas USA;
4
Emeritus, Department of Biology, Midwestern
State University, Wichita Falls, Texas USA
Abstract. The spider Myrmecicultor chihuahuensis Ram´
ırez, Grismado & Ubick (Myrmecicultoridae) was described in
2019 and hypothesized to be a myrmecophile, living inside the nests of Novomessor (Myrmicinae) and perhaps also
Pogonomyrmex (Myrmicinae) ants. To test the hypothesis that M. chihuahuensis are chemical mimics of their host ants, we
carried out behavioral bioassays to observe interactions between the spiders and the host ants. We compared the cuticular
hydrocarbon (CHC) profiles of the spiders and the ants. We discovered that this new species of spider is a myrmecophage,
displaying hunting strategies similar to other myrmecophagous spiders, particularly those in the genus Zodarion
Walckenaer, 1826 (Zodariidae). The CHC profile of M. chihuahuensis did not match the profile of the ants with which it
associates, Novomessor albisetosus (Mayr), but ants and spider shared several compounds, potentially involved in species
recognition.
Keywords: Myrmecophage, Zodarion,Novomessor,Pogonomyrmex, ant guest
https://doi.org/10.1636/JoA-S-21-072
The spider, Myrmecicultor chihuahuensis Ram´
ırez, Grismado, &
Ubick (Myrmecicultoridae) was described in 2019 (Ram´
ırez et al.
2019) (Fig. 1) and was hypothesized to be an ant inquiline. This small
spider has only been found in association with ant nests, specifically
nests of Novomessor albisetosus (Mayr, 1886) (Myrmicinae), N.
cockerelli (Andr´
e, 1893), and Pogonomyrmex rugosus Emery, 1895
(Myrmicinae). Ram´
ırez et al. (2019) and Azevedo et al. (2021) carried
out multi-locus phylogenetic analyses suggesting that M. chihuahuen-
sis does not belong to any known spider family. Therefore, Ram´
ırez et
al. (2019) placed this species in its own family, the Myrmecicultoridae.
Myrmecicultor chihuahuensis shares some morphological similarities
with spiders in the families Zodariidae or Prodidomidae (Ram´
ırez et
al. 2019) but, based on the molecular data, is distinct from those
families.
David Lightfoot observed these mysterious spiders moving on the
mound of a P. rugosus nest in the Chihuahuan Desert in Mexico (fig.
11F in Ram´
ırez et al. 2019). This was the only known instance that
live spiders of this species have ever been observed on the surface of
ant colonies. Lightfoot (pers. comm.) indicated that the spiders
appeared to approach and contact a worker ant using their front legs.
This type of contact has been reported in other species of
myrmecophilous spiders living inside or in close proximity to ant
colonies (Donisthorpe 1927; Allan & Elgar 2001; Erthal & Tonhasca
2001; reviewed in Cushing 1997) and may be a mechanism for
myrmecophiles to acquire the cuticular hydrocarbon (CHC) profile of
host ants (reviewed in Akino 2008, Nash & Boomsma 2008; von
Beeren et al. 2011, 2012a; Parker 2016).
Lightfoot’s observations, the fact that these spiders have only been
collected from pitfall traps placed 0.5 – 1 m from the nest entrances of
ants, and the collection of specimens from soil sifted from excavated
ant nests (see Ram´
ırez et al. 2019) supported the hypothesis that these
spiders are myrmecophiles that live inside nest chambers. It was
further hypothesized in the 2019 paper that these small spiders (adults
slightly ,3 mm in length) are likely feeding on other small
arthropods living inside the colonies as has been demonstrated for
other species of spider myrmecophiles (Porter 1985; Cushing 1995).
To live alongside ants, the spiders either need to evolve behavioral
avoidance strategies, mechanical defense mechanisms, or chemical or
morphological adaptations that allow them to avoid being detected
by the hosts (Lenoir et al. 1999; Cushing 1997, 2012; Geiselhardt et al.
2007; Akino 2008; Ceccarelli 2013; Parmentier et al. 2017; Fischer et
al. 2020; Lorenzi & d’Ettorre 2020). Based on field observations, we
hypothesized that M. chihuahuensis do live closely associated with or
inside the host colonies. We further hypothesized that these spiders
may show some degree of behavioral interaction with the host ants
that could suggest some form of chemical mimicry. To test our
hypotheses, we: (1) carried out behavioral bioassays with living
spiders and host ants to determine the level of behavioral interaction
and (2) compared the CHC profiles of spiders and ants collected from
the same nests in 2019 and 2020 to determine if there was evidence for
chemical mimicry.
In October 2019, we traveled to the Dalquest Desert Research
Station (DDRS) located in the Chihuahuan Desert in Texas, United
States to excavate ant nests and look for spiders inside. During an
excavation of a N. albisetosus nest carried out 23–24 October 2019,
one juvenile M. chihuahuensis and one adult female were collected
from an excavation pit at the DDRS (29.554208N, 103.786408W;
DMNS ZA.41776 in https://scan-bugs.org/portal/index.php). The
one female and juvenile spider along with samples of the respective
host ants from the same colony were flash frozen and sent to AB to
compare the CHC profile of the spiders and the ants. From 28
September to 5 October 2020, we revisited DDRS and used dry pitfall
trap sampling to capture live spiders that could be used for behavioral
bioassays and could also be subsequently sent to AB for CHC
analysis along with additional samples of host ants.
We set six dry pitfall traps 0.5 – 1.0 m from primary nest openings
of N. albisetosus. Each trap consisted of two plastic cups set flush to
the surface of the ground with a smaller plastic cup set inside these
with the bottom cut out; a flat rock was suspended over these cups to
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keep the interior of the trap from overheating in the desert habitat.
Dry pitfall traps (one per nest) were placed at the beginning of the
fieldwork and monitored each morning thereafter to check for
spiders.
Two live female spiders (M. chihuahuensis) were collected from a
single pitfall trap set next to one N. albisetosus nest. No other live
spiders were collected in the vicinity of the remaining nests. Seven N.
albisetosus host ants from the same nest were also collected to use in
the behavioral bioassay. The spiders were introduced into a small
glass Pyrex dish 10 cm
2
x 4 cm deep. A thin layer of soil was placed in
the bottom of this container and a small piece of bark was placed
against one wall to provide a hiding place for the spiders (Fig. 2). At
18:30 in the evening, we began observations of any interactions
between spiders and ants using a red light to reduce disturbance from
light. Since spiders had previously only been recorded on the surface
of ant nests at night (Lightfoot, pers. obs.), it was assumed that this
species was nocturnal.
For the analysis and comparison of CHCs of spiders and their
putative host ants, freeze-killed specimens of potential host ants (10
N. albisetosus from both the 2019 and 2020 trips) and spiders (4 M.
chihuahuensis including the two females from 2020 as well as the
female and juvenile from 2019) were used. The live females and the N.
albisetosus ants collected in 2020 were flash frozen using dry ice after
the behavioral bioassay was completed; the other two spiders
collected in 2019 from excavation pits were also flash frozen with
dry ice and sent to AB for analysis along with host ants.
The flash frozen ants and spiders were submersed in 150 ll hexane
with an internal standard for 20 min. For chemical profiling, we used
a GCMS-QP2020 gas chromatography/mass-spectrometry system
(Shimadzu, Ky¯oto, Japan) equipped with a ZB-5MS fused silica
capillary column (30 m x 0.25 mm ID, df ¼0.25 lm) from
Phenomenex (Torrance, CA, USA). Samples (1 ll for ants and 1 ll
for spiders) were injected using an AOC-20i autosample, into split/
splitless-injector in splitless-mode at a temperature of 3108C. Helium
was used as the carrier-gas with a constant flow rate of 2.13 ml/min.
The start temperature was set to 408C with a 1-minute hold; after that
the temperature was increased 308C/min to 2508C and further
increased 508C/min to a final temperature of 3208C and held for 5
minutes. Electron impact ionization spectra were recorded at 70 eV
ion source voltage, with a scan rate of 0.2 scans/sec from m/z 40 to
650. The ion source of the mass spectrometer and the transfer line
were kept at 2308C and 3208C, respectively. CHCs were identified
using diagnostic ions and retention indices calculated based on a
standard series of n-alkanes (Carlson et al. 1998) and compared to
CHC available for N. cockerelli (Smith et al. 2009). The double bond
positions in alkenes were determined by iodine-catalyzed methyl-
thiolation of double bonds using DMDS (dimethyl-disulfide, Sigma-
Aldrich, St. Louis, MO) and subsequent mass spectrometry according
Figure 1–4.—The myrmecophagous spider Myrmecicultor chihuahuensis (Myrmecicultoridae). (1) Myrmecicultor chihuahuensis male (DMNS
ZA.41782). Scale bar ¼1 mm. (2) 10 310 cm diameter Pyrex dish used for behavioral observations. The small piece of bark provided a hiding
place for the spiders. (3) Circular corrals made from soil granules by Myrmecicultor chihuahuensis females. (4) M. chihuahuensis feeding on
Novomessor albisetosus with fangs inserted behind ant’s head.
CUSHING ET AL.—TROPHIC SPECIALIZATION OF MYRMECICULTOR CHIHUAHUENSIS 251
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to Carlson et al. (1989). For statistical comparison of the CHC
profiles, we used a PERMANOVA analysis on a Bray-Curtis
similarity matrix using species as fixed effect in R 3.6.1 (R Core
Team 2019) based on a previously published code (Br ¨
uckner &
Heethoff 2017).
After introducing the two female spiders to the Pyrex enclosure
(Fig. 2), they built arena-shaped retreats out of sand particles beneath
the wood fragment (Fig. 3) (apparent the morning after introduction
into the enclosure). When the ants were introduced to the enclosure,
both spiders were beneath the wood fragment. Soon after introducing
the ants, the spiders emerged from under the wood, presumably in
response to the ants’ movements in the container. We watched and
filmed several successful hunting sequences under red light so as not to
disrupt the spiders’ behaviors. The behavior of the spiders towards the
ants was consistent: a spider repeatedly approached an ant, quickly
moving away when the ant turned toward the spider (see supplemental
videos 0212-03 and 0215-09, online at https://doi.org/10.1636/JoA-S-
21-072.s1 and https://doi.org/10.1636/JoA-S-21-072.s2 respectively).
In no instance did either spider approach an ant frontally. After
pursuing an ant around the enclosure, the spider rushed at the ant and
bit a rear leg, then retreated (see supplemental video 0215-09). The
effects of the spider’s venom were apparent within a few seconds (See
supplemental video 0215-11, https://doi.org/10.1636/JoA-S-21-072.
s3). The ant’s movement slowed, the body bent, and after a few
minutes, paralysis from the venom was complete. The spider then re-
approached, inserted its fangs behind the ant’s head, lifted, and carried
the ant toward the wood fragment (Fig. 4).
In one hunting sequence, one of the spiders bit a single ant
repeatedly before moving away. We also observed instances when a
live (unbitten) ant approached the encumbered spider. In each of
these instances, when an active ant approached the spider encumbered
with a paralyzed ant, the spider immediately repositioned, turned, or
flipped itself so that the approaching ant would encounter the
paralyzed nest mate, rather than the spider. The spider easily
manipulated the paralyzed ant even though it was larger than the
spider and utilized the dead (or dying) ant as a shield. The spider’s
attack of the host ants could be described as an ambush. In no
instance did we observe any evidence of spiders luring the ants or of
spiders using their front legs to ‘‘pseudo-antennate’’ the hosts as was
suggested by David Lightfoot’s observations in the field.
Comparing the CHC profiles of the spider and the putative host
ants (N. albisetosus), we found 61 compounds from cuticle extractions
(Table 1; Fig. 5), seven of which remain to be elucidated. Sixty of the
compounds were detected for the spider, while we found 42 CHC-
related compounds for N. albisetosus (Table 1). A majority of
compounds was shared by both species including most n-alkanes
(C27–C32), the respective mono-methyl alkanes of similar length (see
Table 1 for details and Fig. 5). The eight CHCs which appeared to be
unique to the spider species included mainly monomethyl and
dimethyl alkanes with a C26 backbone (Table 1). Although the
chemical profiles (Fig. 5) and overall composition of CHCs between
ants and spiders was different (PERMANOVA: N
permu
¼9999;
pseudoF¼4.34; P¼0.0011), both species shared several compounds
in similar ratios (17/61 CHC; ~25%).
It is clear from these observations that M. chihuahuensis is a
myrmecophage. The hunting behavior of this spider is similar to that
reported for other species of myrmecophages (reviewed in Cushing
2012). These spiders avoid frontal attacks, instead approaching ants
from the rear. Their hunting strategy is very similar to that of species
of Zodarion Walckenaer, 1826 (Peka
´r 2004). After paralyzing an ant,
the spider carries and uses it as a shield, presenting the dead ant to
any approaching nest mate. This behavior is very similar to the
hunting strategy noted in various species of Zodarion (Zodariidae)
(Peka
´r & Kra
´l 2002; Couvreur 1990a, b). Such a rear attack and even
the use of dead ants as ‘‘shields’’ has also been noted in several other
genera of myrmecophagous spiders in the family Thomisidae such as
Table 1.—Cuticular hydrocarbons of Novomessor albisetosus and
Myrmecicultor chihuahuensis. The retention indices (RI), identified
CHCs and their mean (6SD) abundances. Double bonds of alkenes
(*) were determined by DMDS derivatization. n.d. denotes non
detected compounds.
RI compound N. albisetosus M. chihuahuensis
2500 C25 1.8861.12 0.7360.62
2536 11-; 13-Me-C25 0.0760.09 0.2960.17
2575 3-Me-C25 0.0960.09 0.6360.67
2600 C26 0.5360.15 1.7661.88
2606 8-Me-C26 n.d. 0.9260.88
2628 10-,14-Me-C26 0.1160.12 0.2460.28
2664 2- or 4-Me-C26 n.d. 0.2460.24
2670 Me-C26 n.d. 0.2160.22
2688 4,12-Dime-C26 n.d. 0.1760.19
2700 C27 4.6162.4 4.8861.78
2731 9-,11-,13-Me-C27 1.7960.82 3.1462.72
2736 Me-C27 0.0660.09 0.3360.23
2742 7-MeC27 0.5460.38 0.960.51
2751 5-MeC27 0.8860.55 0.6760.53
2774 3-MeC27 0.9360.63 4.4365.5
2800 C28 2.1361.14 2.2861.71
2805 3,7-;3,11-Dime-C28 n.d. 1.6761.47
2829 10-,14-Me-C28 0.7560.84 4.765.27
2858 unknown n.d. 0.3960.33
2863 2- or 4-Me-C28 n.d. 0.560.43
2871 meC28 n.d. 0.6760.34
2875 C29-9-ene* 1.7960.39 2.0163.26
2888 4,12-Dime-C28 n.d. 1.6961.17
2900 C29 10.4667.21 3.7562.19
2930 9-,11-,13-,15-Me-C29 2.9760.98 2.5961.26
2939 7-Me-C29 0.8960.57 0.7260.7
2952 5-Me-C29 1.4661.18 0.6160.3
2965 2-Me-C29 n.d. 0.9160.52
2973 3-Me-C29 1.8160.62 1.4960.88
2986 5-,x-Dime-C29 n.d. 0.5160.48
3000 C30 1.2860.28 1.3261.06
3024 10-,14-Me-C30 1.6360.45 1.3760.27
3055 unknown n.d. 0.5560.36
3064 2- or 4-Me-C30 n.d. 0.3660.42
3080 C31-9-ene* 15.1361.55 0.4960.19
3100 C31 1.260.65 5.664.27
3130 9-;11-;13-;15-Me-C31 8.2761.53 5.8861.83
3142 7-Me-C31 1.0861.05 0.9661.06
3153 5-Me-C31 4.0960.62 5.2461.97
3162 unknown 2.2660.67 n.d.
3179 unknown 0.9360.27 1.1360.37
3200 C32 1.0960.12 2.6360.85
3230 10-,14-Me-C32 3.9160.67 3.8261.51
3255 unknown 0.7660.1 2.2563.12
3268 2- or 4-Me-C32 n.d. 0.8561.1
3277 Me-C32 0.1960.14 0.7160.52
3290 C33-ene 0.9360.09 0.460.35
3310 unknown n.d. 0.8160.91
3344 9-;11-;13-;15-Me-C33 9.761.57 7.561.36
3353 7-Me-C33 1.461.58 1.161.3
3371 Dime-C33 2.9660.98 2.9160.82
3388 5-,x-Dime-C33 n.d. 0.2860.24
3400 C34 0.0260.07 0.2760.32
3437 Me-C34 0.3960.19 0.6560.12
3472 Dime-C34 1.6561.03 1.2460.32
3495 unknown 1.3461.43 0.5560.95
3500 C35 n.d. 1.1160.67
3624 10-,14-Me-C36 3.2760.63 2.6561.1
3658 Dime-C36 2.860.4 3.2860.45
3740 9-;11-;13-Me-C37 n.d. 0.0460.08
3750 7-Me-C37 n.d. 0.0260.03
252 JOURNAL OF ARACHNOLOGY
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Aphantochilus rogersi O.P.-Cambridge, 1871 (Piza 1937; Oliveira &
Sazima 1984; Castanho & Oliveira 1997) and Bucranium spp.
(Thomisidae) (Piza 1937; Bristowe 1941; Oliveira & Sazima 1984;
Castanho & Oliveira 1997; reviewed in Cushing 2012). The similarity
in trophic hunting behavior between these spiders in the new family
Myrmecicultoridae and those in the family Zodariidae is particularly
interesting given the observation in Ram´
ırez et al. (2019) that the new
species shares certain morphological characters as those in the family
Zodariidae such as the short posterior spinnerets, the strongly
procurved anterior eye row, and similarities in the leg setae.
The two female spiders killed nine ants in the course of two nights.
All ants added to the Pyrex container were rapidly killed by the
spiders, although they were observed feeding only on one or two of
these ants. This level of carnage, or ‘‘over-kill,’’ has also been
documented for species of Zodarion (Peka
´r 2005; Peka
´r & Toft 2015).
This over-kill is hypothesized to be a strategy related to the
specialized hunting of dangerous prey (L´
ıznarova
´& Peka
´r 2013).
However, it may be an artifact of the small size of the enclosure and
the inability of the spiders or ants to escape one another.
There are many strategies ant symbionts (myrmecophiles and
myrmecophages) use to achieve association with their hosts, ranging
from behavioral adaptations and morphological defense to chemical
mimicry and weaponry (e.g., Akino 2008; Kronauer & Pierce 2011;
von Beeren et al. 2012b; Parker 2016; Parmentier 2019). Here, we
gathered preliminary data to test whether the ant associated spider,
M. chihuahuensis, uses chemical mimicry of its host’s CHCs to live in
close proximity with the ant. We found that the spider CHCs did not
match that of N. albisetosus, but did show some similarity to the
chemical profile of the ants. As with our study, Peka
´r & Jiroˇ
s(2011)
found some similarity in CHC profiles between the myrmecophagous
Zodarion alacre (Simon, 1870) spider that feeds on Iberoformica
subrufa (Roger, 1859) (Formicinae). These authors hypothesized that
the ant-associated CHC compounds found in Z. alacre might be
produced de novo by the myrmecophagous spider. The mechanism by
which M. chihuahuensis acquire their CHCs (or manufacture these
chemical signals) remains unknown. It is also unclear whether or not
the chemical signature of M. chihuahuensis is similar enough to allow
the spider to become fully integrated into the colony or just allow the
spider to hunt these dangerous prey without risk of attack. The eight
CHCs that appear to be unique to the spider profile are likely to
contain enough information content for the ants to recognize M.
chihuahuensis as a foreign organism and elicit a defensive response,
although this also remains to be tested. Novomessor ants are not
particularly aggressive towards non-colony members (Whitford et al.
1980) hence we hypothesize that this non-aggressiveness may enable
the spider to live in close nest proximity even while displaying a
mismatching CHC profile. Like zodariids, this spider may build its
corral-shaped retreats under debris in the vicinity of the nests
(Cushing & Santangelo 2002). Our observations do not support the
hypothesis that these spiders are inquilines.
Many aspects of the natural history of this ant myrmecophage
remain to be discovered including how they locate their host ant
colonies (assuming they are stenophagous and prey only on particular
species of ants). It has been suggested for other species of
myrmecophagous spiders that these specialized stenophagous hunters
may eavesdrop on ant pheromones as a strategy for locating their
prey (Allan et al. 1996; Clark et al. 2000; Ca
´rdenas et al. 2012; Fischer
2019; Adams et al. 2020). It is also unknown what juvenile spiders
feed on. Clearly much remains to be discovered about the biology and
chemical ecology of this interesting new species of myrmecophage.
ACKNOWLEDGMENTS
The authors thank Midwestern State University for allowing access
and use of the Dalquest Desert Research Station during our studies.
Thanks also to Rick Wicker, DMNS photographer, for photograph-
ing the spiders’ arenas and helping with the figure plate.
SUPPLEMENTAL MATERIALS
Video clips taken with iPhone under red light of Myrmecicultor
chihuahuensis females hunting Novomessor albisetosus ants.
Supplemental Video 1 (0212-03) Hunting sequence – spider biting
rear legs of ant, online at https://doi.org/10.1636/JoA-S-21-072.s1
Supplemental Video 2 (0215-09) Hunting sequence – spider
ambushing ant from rear and biting multiple times, online at
https://doi.org/10.1636/JoA-S-21-072.s2
Supplemental Video 3 (0215-11) Effect of spider venom on bitten
ant, online at https://doi.org/10.1636/JoA-S-21-072.s3
LITERATURE CITED
Adams RMM, Wells RL, Yanoviak SP, Frost CJ, Fox EGP. 2020.
Interspecific eavesdropping on ant chemical communication.
Frontiers in Ecology and Evolution 8:1–13, https://www.
frontiersin.org/articles/10.3389/fevo.2020.00024/pdf
Akino T. 2008. Chemical strategies to deal with ants: a review of
mimicry, camouflage, propaganda, and phytomimesis by ants
(Hymenoptera: Formicidae) and other arthropods. Myrmecologi-
cal News 11:173–181.
Allan RA, Elgar MA. 2001. Exploitation of the green tree ant,
Oecophylla smaragdina, by the salticid spider Cosmophasis
bitaeniata.Australia Journal of Zoology 49:129–137.
Allan RA, Elgar MA, Capon RJ. 1996. Exploitation of an ant
chemical alarm signal by the zodariid spider Habronestes bradleyi.
Figure 5.—Cuticular hydrocarbon (CHC) profiles of the spider Myrmecicultor chihuahuensis and Novomessor albisetosus ants. Example gas
chromatographic traces of CHCs extracted from the spider and ant species. Major CHCs are labeled; complete list by retention index can be
found in Table 1.
CUSHING ET AL.—TROPHIC SPECIALIZATION OF MYRMECICULTOR CHIHUAHUENSIS 253
Downloaded From: https://bioone.org/journals/The-Journal-of-Arachnology on 29 Aug 2022
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Proceedings of the Royal Society B 263:69–73, doi.org/10.1098/
rspb.1996.0012
Azevedo GHF, Bourgie T, Carboni M, Hedin M, Ram´
ırez MJ. 2021.
Combining genomic, phenotypic and Sanger sequencing data to
elucidate the phylogeny of the two-clawed spiders (Dionycha).
Molecular Phylogenetics and Evolution 166: 107327, doi.org/10.
1016/j.ympev.2021.107327
Bristowe WS. 1941. The Comity of Spiders II. Ray Society, London,
UK.
Br¨
uckner A, Heethoff M. 2017. A chemo-ecologists’ practical guide to
compositional data analysis. Chemoecology 27:33–46, doi.org/10.
1007/s00049-016-0227-8
Ca
´rdenas M, Jiroˇ
sP, Peka
´r S. 2012. Selective olfactory attention of a
specialised predator to intraspecific chemical signals of its prey.
Naturwissenschaften 99:597–605, doi.org/10.1007/s00114-012-
0938-9
Carlson DA, Bernier UR, Sutton BD. 1998. Elution patterns from
capillary GC for methyl-branched alkanes. Journal of Chemical
Ecology 24:1845–1865, doi.org/10.1023/A:1022311701355
Carlson DA, Roan CS, Yost RA, Hector J. 1989. Dimethyl disulfide
derivatives of long chain alkenes, alkadienes, and alkatrienes for
gas chromatography/mass spectrometry. Analytical Chemistry
61:1564–1571, doi.org/10.1021/ac00189a019
Castanho LM, Oliveira PS. 1997. Biology and behavior of the
neotropical ant-mimicking spider Aphantochilus rogersi (Araneae:
Aphantochilidae): nesting, maternal care and ontogeny of ant-
hunting techniques. Journal of Zoology, London 242:643–650.
Ceccarelli FS. 2013. Ant-mimicking spiders: strategies for living with
social insects. Psyche: A Journal of Entomology 2013 (839181), doi.
org/10.1155/2013/839181
Clark RJ, Jackson RR, Cutler B. 2000. Chemical cues from ants
influence predatory behavior in Habrocestum pulex, an ant-eating
jumping spider (Araneae, Salticidae). Journal of Arachnology28:309–
318, doi.org/10.1636/0161-8202(2000)028[0309:CCFAIP]2.0.CO;2
Couvreur JM. 1990a. Le comportement d’resentation d’un leurre’
chez Zodarion rubidium (Araneae, Zodariidae). Proceedings of the
12
th
European Colloquium of Arachnology, Paris, C´
el´
erier ML,
Heurtault J, Rollard C (eds). Vol. 1, pp. 75–79, Bulletin de la
Soci´
ete Europ´
ıene Arachnologique, Paris, France.
Couvreur JM. 1990b. Quelques aspects de la biologie de Zodarion
rubidium, Simon, 1914. Nieuwsbrief van de Belgische Arachnolo-
gische Vereniging 7:7–15.
Cushing PE. 1995. Description of the spider Masoncus pogonophilus
(Araneae, Linyphiidae), a harvester ant myrmecophile. Journal of
Arachnology 23:55–59.
Cushing PE. 1997. Myrmecomorphy and mymecophily in spiders: a
review. Florida Entomologist 80:165–193.
Cushing PE. 2012. Spider-ant associations: an updated review of
myrmecomorphy, myrmecophily, and myrmecophagy in spiders.
Psyche 2012:1–23, doi.org/10.1155/2012/151989
Cushing PE, Santangelo RG. 2002. Notes on the natural history and
hunting behavior of an ant eating zodariid spider (Arachnida,
Araneae) in Colorado. Journal of Arachnology 30:618–621, doi.
org/10.1636/0161-8202(2002)030[0618:NOTNHA]2.0.CO;2
Donisthorpe H. 1927. The Guests of British Ants, Their Habits and
Life Histories. London: Routledge and Sons.
Erthal M Jr, Tonhasca A Jr. 2001. Attacobius attarum spiders
(Corinnidae): myrmecophilous predators of immature forms of the
leaf-cutting ant Atta sexdens (Formicidae). Biotropica 33:374–376.
Fischer A. 2019. Chemical communication in spiders – a methodo-
logical review. Journal of Arachnology 47:1–27, doi.org/10.1636/
0161-8202-47.1.1
Fischer G, Friedman NR, Huang J-P, Narula N, Knowles LL,
Fischer BL, et al. 2020. Socially parasitic ants evolve a mosaic of
host-matching and parasitic morphological traits. Current Biology
30:3639–3646, doi.org/10.1016/j.cub.2020.06.078
Geiselhardt SF, Peschke K, Nagel P. 2007. A review of myrmecophily
in ant nest beetles (Coleoptera: Carabidae: Paussinae): linking
early observations with recent findings. Naturwissenschaften
94:871–894.
Kronauer DJ, Pierce NE. 2011. Myrmecophiles. Current Biology
21(6), R208–R209.
Lenoir A, Fresneau D, Errard C, Hefetz A. 1999. Individuality and
colonial identity in ants: the emergence of the social representa-
tion concept. Pp. 219–223. In Information Processing in Social
Insects. Birkh¨
auser, Basel., doi.org/10.1007/978-3-0348-8739-7_
12
L´
ıznarova
´E, Peka
´r S. 2013. Dangerous prey is associated with a type
4 functional response in spiders. Animal Behaviour 85:1183–1190,
dx.doi.org/10.1016/j.anbehav.2013.03.004
Lorenzi MC, d’Ettorre P. 2020. Nestmate recognition in social
insects: what does it mean to be chemically insignificant? Frontiers
in Ecology and Evolution 7:488, doi.org/10.3389/fevo.2019.
00488
Nash DR, Boomsma JJ. 2008. Communication between hosts and
social parasites. Pp. 55–79. In Sociobiology of Communication: an
Interdisciplinary Perspective, (d’Ettorre P, Hughes DP, eds.).
Oxford: Oxford University Press,
Oliveira PS, Sazima I. 1984. The adaptive bases of ant-mimicry in a
neotropical aphantochilid spider (Araneae: Aphantochilidae).
Biological Journal of the Linnean Society 22:145–155.
Parker J. 2016. Myrmecophily in beetles (Coleoptera): evolutionary
patterns and biological mechanisms. Myrmecological News 22:65–
108.
Parmentier T. 2019. Guests of social insects. Pp. 1–15. In Encyclo-
pedia of Social Insects. (Starr C, ed). Springer. doi.org/10.1007/
978-3-319-90306-4_164-1
Parmentier T, Dekoninck W, Wenseleers T. 2017. Arthropods
associate with their red wood ant host without matching
nestmate recognition cues. Journal of Chemical Ecology 43:644–
661.
Peka
´r S. 2004. Predatory behavior of two European ant-eating spiders
(Araneae, Zodariidae). Journal of Arachnology 32:31–41.
Peka
´r S. 2005. Predatory characteristics of ant-eating Zodarion
spiders (Araneae: Zodariidae): potential biological control agents.
Biological Control 34:196–203, doi.org/10.1016/j.biocontrol.2005.
05.008
Peka
´r S, Jiroˇ
sP. 2011. Do ant mimics imitate cuticular hydrocarbons
of their models? Animal Behaviour 82:1193–1199, doi.org/10.1016/
j.anbehav.2011.09.007
Peka
´rS,K
ˇ
ra
´l J. 2002. Mimicry complex in two central European
zodariid spiders (Araneae: Zodariidae): how Zodarion deceives
ants. Biological Journal of the Linnean Society 75:517–532, doi.org/
10.1046/j.1095-8312.2002.00043.x
Peka
´r S, Toft, S. 2015. Trophic specialisation in a predatory group:
the case of prey-specialised spiders (Araneae). Biological Reviews
90:744–761, doi.org/10.1111/brv.12133
Piza S de T. 1937. Novas esp´
ecies de aranhas myrmecomorphas do
Brazil e considera¸c˜
oes sobre o seu mimetismo. Revista do Museu
Paulista 23:307–319.
Porter SD. 1985. Masoncus spider: a miniature predator of
Collembola in harvester ant colonies. Psyche 92:145–150.
R Development Core Team. 2019. R: A Language and Environment
for Statistical Computing. Vienna, Austria: R Foundation for
Statistical Computing.
Ram´
ırez MJ, Grismado CJ, Ubick D, Ovtsharenko V, Cushing PE,
Platnick NI, et al. 2019. Myrmecicultoridae, a new family of
myrmecophilic spiders from the Chihuahuan Desert (Araneae:
Entelegynae). American Museum Novitates 3930:1–24.
Smith AA, H¨
olldobler B, Liebig J. 2009. Cuticular hydrocarbons
reliably identify cheaters and allow enforcement of altruism in a
254 JOURNAL OF ARACHNOLOGY
Downloaded From: https://bioone.org/journals/The-Journal-of-Arachnology on 29 Aug 2022
Terms of Use: https://bioone.org/terms-of-use

social insect. Current Biology 19:78–81, doi.org/10.1016/j.cub.2008.
11.059
von Beeren C, Hashim R, Witte V. 2012a. The social integration of a
myrmecophilous spider does not depend exclusively on chemical
mimicry. Journal of Chemical Ecology 38:262–271.
von Beeren C, Pohl S, Witte V. 2012b. On the use of adaptive
resemblance terms in chemical ecology. Psyche 2012: 635761.
von Beeren C, Schulz S, Hashim R, Witte V. 2011. Acquisition of
chemical recognition cues facilitates integration into ant socie-
ties. BMC Ecology 11(1):30, https://doi.org/10.1186/1472-6785-
11-30.
Whitford WG, Depree E, Johnson P. 1980. Foraging ecology of two
Chihuahuan Desert ant species: Novomessor cockerelli and
Novomessor albisetosus.Insectes Sociaux 27:148–156.
Manuscript received 12 November 2021, revised 13 January 2022,
accepted 11 February 2022.
CUSHING ET AL.—TROPHIC SPECIALIZATION OF MYRMECICULTOR CHIHUAHUENSIS 255
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