Content uploaded by Luis M. Mejía-Ortíz
Author content
All content in this area was uploaded by Luis M. Mejía-Ortíz on Dec 20, 2017
Content may be subject to copyright.
© The Author 2017. Published by Oxford University Press on behalf of The Crustacean Society. All rights reserved.
For permissions, please e-mail: journals.permissions@oup.com
Journal of Crustacean Biology
Journal of
Crustacean Biology
Journal of Crustacean Biology (2017) 1–7. doi:10.1093/jcbiol/rux098
The Crustacean Society
Predatory behavior of the cave shrimp Creaseria morleyi
(Creaser, 1936) (Caridea: Palaemonidae), the blind hunter
of the Yucatán cenotes, Mexico
Efraín M.Chávez-Solís1,3, Luis M.Mejía-Ortíz2 and NunoSimões3,4,5
1Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Copilco-Universidad, Ciudad de México 04510, México;
2Laboratorio de Bioespeleología y Carcinología, Universidad de Quintana Roo, Av. Andrés Quintana Roo s/n, Cozumel 77600, Quintana Roo, México;
3Unidad Multidisciplinaria de Docencia e Investigación, Facultad de Ciencias, Universidad Nacional Autónoma de México, Sisal 97355, Yucatán, México
4Laboratorio Nacional de Resiliencia Costera, Unidad Académica de Yucatán, Universidad Nacional Autónoma de México, Sisal, 97355, Yucatán, México; and
5International Chair for Coastal and Marine Studies in Mexico, Harte Research Institute for Gulf of Mexico Studies, Texas A&M University-Corpus Christi, 6300 Ocean Drive,
Unit 5869, Corpus Christi, Texas 78412, USA
Correspondence: N.Simoes; e-mail: ns@ciencias.unam.mx
(Received 14 March 2017; accepted 5 October 2017)
ABSTRACT
Recent studies of the trophic structure of the underwater cave ecosystems in the Yucatán
Peninsula have regarded the largest crustacean inhabitant, the blind palaemonid shrimp
Creaseria morleyi (Creaser, 1936), as a scavenger and predator without any evidence on the
behavior of the shrimp. The predatory behavior of C. morleyi is here described for the first
time, verifying its classification as a predator. A variety of prey targets, including the atyid
shrimp Typhlatya sp., were used to demonstrate predation and saprophagous feeding behavior
in C. morleyi using in vitro and in situ observations. Scanning electron microscope images show
the structures of the antennules and antennae that could be responsible for prey detection.
Findings show that C. morleyi is capable of hunting a variety of prey, most likely depending on
their relative size. Observations on the feeding strategy of C. morleyi suggest any animal within
a particular size range is a potential prey, including its own species, which suggests the hy-
pothesis that growth may be favored in early stages of life in order to reach a size refuge from
predation. These observations provide information of some of the adaptations necessary for
a predator to thrive in an aphotic and oligotrophic environment.
Key Words: anchialine environment, cave adaptations, decapods, feeding strategies,
stygofauna
INTRODUCTION
The diversity and biomass of the Yucatán Peninsula underwater,
cave-restricted fauna (stygofauna) is dominated by 47 crustacean
species out of a total of 49 freshwater and anchialine species cur-
rently described (Álvarez & Ilie, 2008; Álvarez et al., 2015; Mejía-
Ortíz et al., 2017). These numbers exclude some exceptional caves
in Cozumel island that host a number of echinoderm, polychaete
stygofauna and other marine stygoxene species (Trujillo Pisanty et al.,
2010; Frontana-Uribe & Solís-Weiss, 2011; Bribiesca-Contreras et
al., 2013). The top stygobiont predators in the freshwater portion of
the anchialine ecosystems are the palaemonid shrimp Creaseria morleyi
(Creaser, 1936) and two species of fishes, Typhliasina pearsei (Hubbs,
1938) and Ophisternon infernale Hubbs, 1938 (Pohlman et al., 2000). The
shrimp is widely distributed in Yucatán caves (Pérez Aranda, 1983;
Botello, 2007). Although the trophic level of C. morleyi has been
assessed through indirect measurements (Pohlman et al., 1997), no
prior visual evidence of its predatory behavior had been previously
reported.
The trophic structure of anchialine ecosystems is relatively
simple and composed of a small number of levels with fewer spe-
cies than most epigean habitats. Pohlman et al. (2011) suggested
only three trophic levels: producers (photosynthetic and chemo-
synthetic), primary and detrital consumers, and generalist or
opportunistic predators and scavengers. Nutrients and organic
matter (e.g., plant or animal detritus and feces) can reach anchi-
aline systems by several processes: lixiviation or filtration of the
surrounding soil into the natural sinkhole, or cenote, and aquifer
Downloaded from https://academic.oup.com/jcb/advance-article-abstract/doi/10.1093/jcbiol/rux098/4706304
by guest
on 10 December 2017
CHÁVEZ-SOLÍS ETAL.
2
(Pohlman et al., 2000), carried by other animals (bats, birds,
humans), or produced within the cenotes or caves. Primary pro-
duction is limited in the anchialine ecosystems and is generated
mainly by chemosynthetic prokaryotes in the aphotic areas of the
caves (Pohlman, 2011). The great majority of cave systems in the
Yucatán Peninsula are flooded. The well or sinkhole that is formed
by the collapse of the surface limestone that exposes the aquifer
is regionally called cenote, a word derived from the Mayan dzonot
(Schmitter-Soto et al., 2002). The morphology of each cenote
governs the amount of light that reaches the water surface, which
is the only place, in the otherwise underground system, where
photosynthesis may occur.
Primary consumer stygofauna in Yucatán is mainly composed
of crustaceans having specialized filtering or scavenging feed-
ing strategies (Mejía-Ortíz et al., 2013), either on the benthos or
the water column. Some anchialine isopods (family Cirolanidae)
tend to be omnivores, display cannibalism, and feed on carcasses
and other organic material deposited on the sediment (Pohlman
et al., 1997). Others, like the mysid Antromysis (Antromysis) cenoten-
sis Creaser, 1936 and the thermosbaenacean Tulumella unidens
Bowman & Ilie, 1988, filter organic matter and microbes sus-
pended in the water column. Atyid shrimps (such as Typhlatya) dis-
play water-column filtering as well as sediment-scraping strategies
(Pohlman et al., 1997; Mejía-Ortíz et al., 2006). Under the halo-
cline, the marine cave systems are inhabited by other predators
such as remipedes (Xibalbanus spp.), which feed on other anchial-
ine crustaceans that may also live in the marine portion of these
caves.
The stygofauna has adapted to dierent cave conditions, which
result in convergent traits. The stygofauna generally has high tol-
erance to long starvation periods through reduction of metabolic
rate (Hervant etal., 1999, 2001; Bishop etal., 2004), increased lon-
gevity (Vogt, 2012), delay of reproduction, reduction in the num-
ber of eggs (Culver & Pipan, 2009), changes in behavioral traits
(Abele & Felgenhauer, 1985; Carpenter, 1999; Friedrich, 2013),
loss of pigmentation and eye structures, and the development
of other sensory organs and structures (Mejía-Ortíz & Hartnoll,
2006; Mejía-Ortíz etal., 2013). Feeding behavior and strategies of
stygobiont predators like C.morleyi have hardly been investigated,
although feeding (or fasting) is one of the most powerful drivers of
evolution (Sket, 1996).
In the extensive groundwater habitats of Yucatán Peninsula,
which have an overall constant environment with only subtle sea-
sonal changes in most abiotic variables, simplified trophic chains
with low biological diversity, and biomass with reduced numbers
of small individuals, the probability of encounters between prey
and predator could be one of the crucial aspects of feeding suc-
cess. Optimal foraging theory predicts an optimization of the
energy input for the energy spent searching, chasing, capturing,
and ingesting prey (Charnov, 1976; Pyke et al., 1977).
We demonstrate that C.morleyi is an eective predator that can
anticipate prey movement and is capable of precise and ecient
attack on their prey, either starting from a still or a moving pos-
ition. We present scanning electron microcopy (SEM) images of
structures on the antennules (A1) and antennae (A2) that could
be involved in prey detection as well as video recordings of in
vitro and in situ predation showing the prey-capture behavior of
C.morleyi.
METHODS
In vitro observations
Six individuals of C.morleyi and 18 of Typhlatya sp. were collected
from the Nayah cenote (20.646513°N, –89.404690°W) following
Mexican regulations (NOM126; collection permit SEMARNAT,
no. SGPA/DGVS: 05263/14) during several night dives on 17
March 2014 at depths of 18 to 33 m using cave-diving techniques.
A system of five 12 l glass aquaria was built to keep experimen-
tal shrimps under observation at Unidad Académica de Yucatán,
Universidad Nacional Autónoma de México (UNAM), Sisal,
Yucatán (Fig. 1): one experimental aquarium with both species,
three holding aquaria to only keep C.morleyi individuals, and one
to keep Typhlatya sp. Each aquarium contained approximately
200g of sediment from the cenote, a small karst rock, and a con-
tinuous water flow from a 150 l reservoir of water collected from
cenote Yaal Utsil (20.623889°N, –89.606667°W). Central aeration
was provided in the 150 l reservoir. Room temperature was kept
at 27°C in accordance to temperature recorded at the site. The
room was permanently kept in total darkness. Four closed-circuit
surveillance infra-red cameras (CCTV-131, Steren Electronics,
China) and two commercial infra-red lights (Steren CCTV-450)
(Fig.1) were installed to record the experimental aquarium at dif-
ferent angles.
Individuals of Typhlatya sp. were placed together in an aquar-
ium, whereas those of C. morleyi were distributed among three
aquaria, each separated by a dividing mesh. Shrimps were fed
with commercial Purina® (Camaronina Agribrands, Ciudad
Obregón, México) penaeid-shrimp pellets once a day.
Experimental observations began 48 h after relocation of
shrimps to the laboratory: one individual of C. morleyi and one
of Typhlatya sp. were transferred into the experimental aquarium
for continuous 24h filming. The process was repeated with other
individuals of the two species for the following two days. Aquaria
were examined each day and the remaining individuals returned
to their respective holding tanks. Atotal of 120 h (5 d) from the
three infra-red cameras were reviewed: 24h of film every time we
transferred a Typhlatya individual into the experimental aquarium,
with a total of five replicates. Three replicates were with complete,
unharmed C.morleyi individuals and two with individuals that lost
one or both of their second pair of pereiopods during capture and
handling.
In situ observations
In situ videos were filmed using GoPro Hero 4 silver at 1080
pixels, narrow view, at 60 frames per second, mounted on two
underwater SolaDive2000 film lights. The first two predatory
interactions were filmed in cenote San Juan, Homún, Yucatán
(20.734056°N, –89.288500°W) at 18 m and 22 m depth, respect-
ively, on 2 November 2016, whereas the third filmed inter-
action was recorded in cenote Kankirixché, Abalá, Yucatán
(20.637235°N, –89.632969°W) at a depth of 24 m on 6 April
2016. All video recordings shown in the supplementary mater-
ial (see below) were made in the twilight zone of the cavern. The
films were made during over 70 dives and a total of 90 h from
20 dierent cenotes in Yucatán Peninsula. When feeding bouts
were recorded, the video clips were cut and edited using GoPro
Studio® software (www.gopro.com) and sent for post-production
editing to VisualMates (www.visualmates.mx).
Scanning electron microscopy
Two individuals of C. morleyi were captured from Cueva Pamul,
Playa del Carmen, Quintana Roo, México for observation.
Preparations used protocols modified from Felgenhauer (1987) and
viewed under a Hitachi Scan Electron 2460 microscope (Hitachi,
Tokyo) at Instituto de Biología, Universidad Nacional Autónoma
de México, Mexico City. The antennular (A1) and antennal (A2)
flagella (as defined by Garm, 2004) were selected for imaging con-
sidering them the main chemical and mechanical receptors as
described for other cave crustaceans (Mejía-Ortíz et al. 2006, 2013).
Downloaded from https://academic.oup.com/jcb/advance-article-abstract/doi/10.1093/jcbiol/rux098/4706304
by guest
on 10 December 2017
PREDATORY BEHAVIOR OF CAVE SHRIMP
3
RESULTS
Individuals of C. morleyi were observed constantly moving dur-
ing field observations, both on the cave bottom and in the water
column. When on the bottom, they moved mostly in a straight line
in an apparent random direction, beating their pleopods with the
abdomen slightly lifted as they walked touching the ground with
the third to fifth pereiopods (Fig. 2A, B). The second pereiopods
were held parallel to the ground and the chelae were always open.
The second pereiopods were laterally extended (Fig. 2A) resulting
in the pereiopods being at right angles, or slightly bent forward
(Fig. 2B). Individuals observed swimming in the water column also
exhibited rapid, rhythmic movement of the pleopods but retracted
their pereiopods under the cephalothorax, except for the first and
second, which were extended forward with chelae opened (Fig.
2C).
Several predatory interactions were observed in the laboratory,
but only one event was filmed (Supplementary material Video S1).
Other predation events were not recorded but the prey was con-
firmed as individuals of Typhlatya sp. No body parts of the latter
were found in aquaria.
Individuals of the two species moved frequently after being
relocated to the observation aquarium but reduced the swim-
ming eorts after 20–60 min. Activity was observed periodically
in Typhlatya sp., with individuals spending most of the time settled
on the aquarium wall and bottom or swimming short distances
in the water column. Individuals of C. morleyi showed greater ac-
tivity than Typhlatya sp. individuals, and although the aquaria were
covered and the room was kept in complete darkness, C. morleyi
individuals increased their activity after sundown by continually
moving across the aquaria.
The in vitro observation involved an individual of C.morleyi (total
length (TL) 61mm) and an individual of Typhlatya sp. (TL 16mm;
the “prey”) (Supplementary material Video S1). Before the attack,
around dawn, both individuals increased their movements and
started to swim around the aquarium. Their movements included
“rest” stops of a few seconds between bouts of swimming. During
several times, the individual of C. morleyi stopped at exactly the
same location where the prey individual had rested. Before the
final approach, both shrimps stopped about 10cm apart, then the
prey began to swim until it sharply changed direction after ap-
parently being touched by the antennal (A2) flagella of C.morleyi
at a distance of approximately 6cm. Only a fraction of a second
after the sharp change in direction of the prey, C. morleyi began
the attack from a stationary position. It quickly turned its body
towards the contact direction and leaped up and forward from
the bottom using its third to fifth pereiopods. Once in the water
column, it swam towards the prey using its pleopods, tail, and ab-
domen until finally it captured the prey in its extended left second
pereiopod chela (Supplementary material VideoS1).
Once captured, the prey was held with the chelae of the second
pereiopod and ripped apart with the chelae of the first pair of
pereiopods, which transferred the food to the mouth. The preda-
tor sank to the bottom and continued feeding. These events took
place in less than one second and the total distance covered by
the predator was approximately 8cm from the beginning of the
attack until the predator settled on the bottom.
Other individuals of C.morleyi that had lost their second pair of
pereiopods, showed a similar attack behavior when placed under
the same conditions, but in all their attempts the Typhlatya sp.
individuals escaped. Although such predatory behavior had been
observed several times in the wild, we only video recorded three
capture events (Supplementary material VideoS2-4).
The predation event filmed in cenote San Juan, Homun
(Supplementary material Video S2) shows an individual of C.mor-
leyi walking on the cenote bottom when it suddenly stretched the
Figure 1. Aquaria, infrared cameras, lights, recorder, and monitor set-up used for recording behavior of Creaseria morleyi (large crustacean) and Typhlatya sp.
(small crustacean).
Downloaded from https://academic.oup.com/jcb/advance-article-abstract/doi/10.1093/jcbiol/rux098/4706304
by guest
on 10 December 2017
CHÁVEZ-SOLÍS ETAL.
4
chela of its right second pereiopod and caught a smaller crust-
acean that had passed in front of it. The prey was most likely the
mysid Antromysis cenotensis or an unidentified crustacean larva. The
slow-motion sequence shows the prey struggling unsuccessfully to
get free with a series of tail flips, with the predator continuing to
move while eating itsprey.
A second video from cenote San Juan (Supplementary material
video S3) shows another C. morleyi individual holding a captured
Typhlatya sp. with the chelae of its first and second pereiopods
while swimming. The capture process was not observed, but on-
site observations revealed the individual of Typhlatya sp. was still
alive during the filming.
Video from cenote Kankirixche (Supplementary material
video S4) shows an individual of C. morleyi capturing and feed-
ing on a small crustacean, most likely A. cenotensis or a crustacean
larva. The attack began with the predator walking on the bot-
tom when suddenly it stopped at about 2.5 body lengths from its
prey, turned, and advanced directly towards it. Once it reached
its prey, the predator caught the smaller crustacean with the che-
lae of its second pair of pereiopods. The prey tried to free itself
with a series of approximately nine tail flips in a fraction of a
second, but failed. The C. morleyi individual then moved back-
wards with three consecutive tail flips and placed the prey into
position in front of its mouthparts, holding it with the chelae
of both pereiopods, then continued walking towards its original
direction.
Scanning electron microscopy (SEM) of the antennae (A2) of
C.morleyi (Fig.3A, B) shows the absence of setae on the first arti-
cles. The outer antennular (A1) ramus, however, has two rows of
four well-defined, short aesthetascs with flattened ends from the
third to the fourth article (Fig.3C, D). Creaseria morleyi has no setae
or pores on the eyes that could function as aids for sensing move-
ment as reported for other cave crustacean species (Mejía-Ortíz &
Hartnoll, 2006; Mejía-Ortíz etal., 2013).
DISCUSSION
Anchialine ecosystems are considered oligotrophic environments
(Schmitter-Soto et al., 2002; Pohlman, 2011; Torres-Talamante
et al., 2011; Derrien et al., 2015) except for cave entrances and
cenotes, which are exposed to sunlight where photosynthetic pri-
mary production occurs. The light-less portions of these caves
typically support low population densities, resulting in very low
probabilities for predators to encounter prey. The stygofauna have
a variety of adaptations for survival in the anchialine environ-
ment (Bishop etal., 2004; Bishop & Ilie, 2012; Culver & Pipan,
2013; Mejía-Ortíz etal., 2013), with food scarcity being one of the
most crucial evolutionary pressures (Sket, 1996). We confirm that
C.morleyi is a generalist top predator that has evolved feeding strat-
egies adapted to live in an anchialine environments.
The most common prey in Yucatán anchialine systems are typ-
ically mysids, thermosbaenaceans, and small caridean shrimps
such as Typhlatya sp. These species are pelagic, benthic, or bentho-
pelagic consumers that feed on organic matter and microbes
(Pohlman et al., 2000). Predation in C. morleyi begins with individu-
als resting at the bottom, suggesting that it is an ambush preda-
tor. The in situ recordings nevertheless show the opposite, with C.
morleyi moving around continuously searching and capturing prey.
The attack strategy starts with ambulatory search behavior show-
ing that the shrimp is capable of capturing prey while swimming.
Swimming behavior suggests that C. morleyi invests a consider-
able amount of energy to encounter prey. The area covered when
moving forward is increased by spreading the second pereiopods
laterally. Swimming through the water column increases the pos-
sibility of encounters with pelagic prey such as A. cenotensis, and
it is more likely to encounter benthic or benthopelagic species,
such as Typhlatya sp., when moving on the substrate. This constant
motion could also be the result of avoidance of the diver’s pres-
ence with the associated impact of air bubbles and light. We were
nevertheless able to capture successful feeding behavior on film,
Figure2. Creaseria morleyi in the wild: A) standing still in cenote Tza Itza at a depth of 12 m deep (31 August 2015); B) walking on the sediment in cenote Tza
Itza at a depth of 18 m at the far end of the cavern (31 August 2015); C) swimming close to a rock in cenote Dzombakal at a depth of 14 m at the entrance
of the cave passage (7 October 2014); D) swimming in the water column at a depth of 14 m, with pleopods 3–5 close to the body and the second pair of
pleopods extended forward, cenote Kanun (4 June 2016). This figure is available in color at Journal of Crustacean Biology online.
Downloaded from https://academic.oup.com/jcb/advance-article-abstract/doi/10.1093/jcbiol/rux098/4706304
by guest
on 10 December 2017
PREDATORY BEHAVIOR OF CAVE SHRIMP
5
indicating some tolerance to such disturbances. The linear trajec-
tories described in the wild could not be observed in the aquarium
due to the obvious size limitations. In vitro behavior was that of a
“lie in wait” predator, which could be an alternative strategy to
find prey in the stable and quiet cave environment.
SEM analysis showed a low density of setae on the antennae
of C. morleyi (Fig.3) compared to other freshwater decapods (see
Mejía-Ortíz & Hartnoll, 2005; Mejía-Ortíz et al., 2006, 2013).
Perhaps this is compensated with a high density of short, flat-
ended aesthetascs on the articles of the antennules similar to those
reported from other anchialine species belonging to several fami-
lies (Mejía-Ortíz et al., 2013). The main function of the antennae
and antennule complex are to increase sensitivity to vibrations and
chemical signals (Mejía-Ortíz et al., 2006). Epigean crustaceans
rely on both vision and olfactory cues for intraspecific interac-
tions, feeding, and reproduction (Delgado-Morales et al., 2004).
Stygobionts rely only on mechanical and chemical inputs in the
aphotic environment. Evidence from cenote Kankirixche shows
C.morleyi sharply changing direction towards its prey at a distance
greater than twice its body length, which is usually the length of
the antennal flagellum (Creaser, 1936). We propose that the anten-
nae and antennules are paramount for eectively sensing the prey
and making the final precise approach to capture theprey.
Creaseria morleyi has been reported to exhibit cannibalism
(Creaser, 1936; Hobbs & Hobbs, 1976; Ilie, 1993), a behavior
confirmed during our collections, when large individuals were
observed eating smaller ones. Cannibalism could indicate a selec-
tion pressure in favor of rapid growth to a large size at the expense
of a delay in reproduction, as reported in other cave crustaceans
that reproduce at a larger size and older age (Cooper, 1975; ref-
erences in Vogt, 2012). Creaseria morleyi could be an example for
the size-refuge hypothesis (Paine, 1976). When small, the shrimp
could be preyed on by its larger conspecifics or fish predators
(in this case Typhliasina pearsei (Hubbs, 1938), Ophisternon infernale
Hubbs, 1938, or Rhamdia guatemalensis (Günther, 1864)), but after
it reaches a certain size it might lack any natural predators, thus
becoming a top predator.
Creaseria morleyi has been observed feeding on bat and bird
excrement, is known to be attracted to baited traps, and even
feed on the cave fish T. pearsei (E. Sosa, pers. com.), although it
is not clear if the fish was captured alive. There is therefore evi-
dence the shrimp is a generalist that could act as an opportun-
istic scavenger. Our observations suggest that it can choose its
prey depending on the relative predator-prey size; as the predator
grows the targeted prey gets bigger as well. Multiple feeding strat-
egies could therefore allow the shrimp to feed on a variety of prey
and exhibit both predatory and saprophagous feeding as stated
by E.Racovitza (in Culver & Pipan, 2013: 51), “many subterra-
nean organisms are carnivores by predilection but saprophagous
by necessity.”
Feeding behavior, previous reports of C. morleyi as a generalist
predator (Pohlman etal., 1997), and seemingly sensitive antennae
and antennules could explain that this species is one of the larg-
est crustacean anchialine predators. The low probabilities of prey
encounters in most oligotrophic cave environments could have
resulted in C. morleyi evolving behaviors that improve the likeli-
hood of prey encounters, the ability to feed on a variety of prey
species, an eective capture behavior, and possibly saprophagy.
Although our observations demonstrate that C. morleyi can
attack, capture, and eat Typhlatya sp. and A. cenotensis, still the fre-
quency of the predatory, saprophagy, and cannibalistic behaviors
as well as the factors that trigger each remain unknown.
Future studies of stomach content, using genomic analysis or
stable isotope food-web tracing, together with chemosensory
experiments, underwater field observations using rebreathers or
infrared cameras and lighting to avoid perturbation, will help elu-
cidate how prey is captured and which types are most commonly
captured and ingested by C. morleyi.
SUPPLEMENTARY MATERIAL
Supplementary material is available in Journal of Crustacean Biology
online and dryad.org (doi:10.5061/dryad.rv801).
Figure3. Scanning electron micrographs of Creaseria morleyi: A) antennule (A1), inner flagellum (i.f) and outer flagellum (o.f); B) antennal (A2) flagellum;
C) base of antennular (A1) outer flagellum; D) antennule (A1) with eight setae per article on the outer flagellum. Arrows in C and D indicate aesthetascs.
Downloaded from https://academic.oup.com/jcb/advance-article-abstract/doi/10.1093/jcbiol/rux098/4706304
by guest
on 10 December 2017
CHÁVEZ-SOLÍS ETAL.
6
S1 Video (first video sequence). In vitro experimentation, C. morleyi
captures and feeds on a Typhlatya sp. individual in an aquarium
(0:00 to 01:22).
S2 Video (second video sequence). In situ observation of C. morleyi
capturing a small crustacean (possibly A. cenotensis) in the cavern
area of cenote San Juan (1:24 to 2:27).
S3 Video (third video sequence). In situ observation of C. morleyi
swimming with a captured Typhlatya sp. individual in its second
pereiopod chelae in the cavern area of cenote San Juan (2:28 to
2:53).
S4 Video (fourth video sequence). In situ observation of C. morleyi
capturing a small crustacean (possibly A. cenotensis) in cenote
Kankirixche (2:54 to 4:41).
ACKNOWLEDGEMENTS
This work was funded by PAPIIT-DGAPA-UNAM-IN222716.
EMCS acknowledges a scholarship from Consejo Nacional de
Ciencia y Tecnología (CONACYT) (294499) for a M.Sc. at
Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma
de México. Photographs in Figure2 are courtesy of Isaí Domínguez
(A, B) and Benjamín Magaña (C, D). The authors thank Berenit
Mendoza Garfias (IB-UNAM) for her help with the SEM analysis,
Gemma Martínez Moreno for her help in the aquaria design and
maintenance, and Julio Duarte Gutiérrez and Ricardo González
Muñoz for their help in the expeditions. The authors appreciate
comments by the editors and two anonymous reviewers whose
comments substantially improved the manuscript.
REFERENCES
Abele, L.G. & Felgenhauer, B.E. 1985. Observations on the ecology and
feeding behavior of the anchialine shrimp Procaris ascensionis. Journal of
Crustacean Biology, 5: 15–24.
Álvarez, F. & Ilie, T.M. 2008. Fauna anquihalina de Yucatán. In:
Crustáceos de México. Estado actual de su conocimiento (F. Álvarez & G.A.
Rodríguez Almaraz, eds.), pp. 379–418. Universidad Autónoma de
Nuevo León, Monterrey, México.
Álvarez, F., Ilie, T.M., Benítez, S., Brankovits, D. & Villalobos, J.L. 2015.
New records of anchialine fauna from the Yucatan Peninsula, Mexico.
Check List, 11: 1–10.
Bishop, R.E. & Ilie, T.M. 2012. Ecological physiology of the anchialine
shrimp Barbouria cubensis: Acomparison of epigean and hypogean pop-
ulations. Marine Biodiversity, 42: 303–310.
Bishop, R.E., Kakuk, B. & Torres, J.J. 2004. Life in the hypoxic and anoxic
zones: Metabolism and proximate composition of Caribbean troglo-
bitic crustaceans with observations on the water chemistry of two
anchialine caves. Jour nal of Crustacean Biolog y, 24: 379–392.
Botello, A. 2007. Variación morfológica y genética en Creaseria morleyi
(Decapoda: Palaemonidae) de la peninsula de Yucatán. Thesis. Universidad
Nacional Autónoma de México, Ciudad de México.
Bowman, T.E. & Ilie, T.M. 1988. Tulumella unidens, a new genus
and species of thermosbaenacean crustacean from the Yucatan
Peninsula, Mexico. Proceedings of the Biological Society of Washington,
101: 221–226.
Bribiesca-Contreras, G., Solís-Marín, F.A., Laguarda-Figueras,
A., Zaldívar-Riverón, A. 2013. Identification of echinoderms
(Echinodermata) from an anchialine cave in Cozumel Island, Mexico,
using DNA barcodes. Molecular Ecology Resources, 13: 1137–1145.
Carpenter, J.H. 1999. Behavior and ecology of Speleonectes epilimnius
(Remipedia, Speleonectidae) from surface water of an anchialine cave
on San Salvador island, Bahamas. Crustaceana, 72: 979–991.
Charnov, E.L. 1976. Optimal foraging, the Marginal Value Theorem.
Theoretical Population Biology, 9: 129–136.
Chavez-Solis, E.M. & Simoes, N. 2017. Predator behavior of cave palae-
monid shrimp, Creaseria morleyi (Creaser, 1936)of Yucatán cenotes: the
blind hunter. Dr yad Digital Repository [doi:10.5061/dryad.rv801].
Cooper, J. 1975. Ecological and behavioral studies in Shelta Cave, Alabama, with
emphasis on decapod crustaceans. Ph.D. thesis. University of Kentucky,
Lexington, KY.
Creaser, E.P., 1936. Crustaceans from Yucatan. In: The cenotes of Yucatan.
A zoological and hydrographic survey (A.S. Pearse, E.P. Creaser & F. Hall,
eds.), pp. 117–132. Carnegie Institution of Washington, Washington,
DC.
Culver, D.C. & Pipan, T. 2009. Adaptations to subterranean life. In: Biology
of caves and other subterranean habitats (D.C. Culver & T. Pipan, eds.), pp.
109–130. Oxford University Press, Oxford, UK.
Culver, D.C. & Pipan, T. 2013. Subterranean ecosystems. In: Encyclopedia
of biodiversity (S. Levin, ed.), pp. 49–62., Waltham, MA.
Delgado-Morales, G., Hernández-Falcón, J. & Ramón, F. 2004. Agonistic
behavior in crayfish: the importance of sensory inputs. Crustaceana, 77:
1–24.
Derrien, M., Árcega-Cabrera, F., Velázquez-Tavera, N.L., Kantún-
Manzano, C.A., & Capella-Vizcaíno, S. 2015. Sources and distribution
of organic matter along the ring of cenotes, Yucatan, Mexico: Sterol
markers and statistical approaches. Science of the Total Environment, 511:
223–229.
Felgenhauer, B.E. 1987. Techniques for preparing crustaceans for
Scanning Electron Microscopy. Journal of Crustacean Biology, 7: 71–76.
Friedrich, M. 2013. Biological clocks and visual systems in cave-adapted
animals at the dawn of speleogenomics. Integrative and Comparative
Biology, 53: 50–67.
Frontana-Uribe, S.C. & Solís-Weiss, V. 2011. First records of polychaetous
annelids from Cenote Aerolito (sinkhole and anchialine cave) in
Cozumel Island, Mexico. Journal of Cave and Karst Studies, 73: 1–10.
Garm, A. 2004. Revising the definition of the crustacean seta and setal
classification systems based on examinations of the mouthpart setae
of seven species of decapods. Zoological Journal of the Linnean Society
(London), 142: 233–252.
Hervant, F., Mathieu, J. & Barré, H. 1999. Comparative study on the
metabolic responses of subterranean and surface-dwelling amphi-
pods to long-term starvation and subsequent refeeding. Jour nal of
Experimental Biology, 202: 3587–3595.
Hervant, F., Mathieu, J. & Durand, J. 2001. Behavioural, physiological and
metabolic responses to long-term starvation and refeeding in a blind
cave-dwelling (Proteus anguinus) and a surface-dwelling (Euproctus asper)
salamander. Journal of Experimental Biology, 204: 269–281.
Hobbs, H.H. III & Hobbs, H.H. Jr. 1976. On the troglobitic shrimps of the
Yucatan Peninsula, Mexico (Decapoda: Atyidae and Palaemonidae).
Smithsonian Contributions to Zoology, 240: 1–23.
Ilie, T.M. 1993. Fauna troglobia acuática de la Península de Yucatán.
In: Biodiversidad marina y costera de México (S.I. Salazar-Vallejo &
N.E. González, eds.), pp. 673–686. Comisión Nacional para el
Conocimiento y Uso de la Biodiversidad (CONABIO) y Centro de
Investigaciones de Quintana Roo (CIQRO), Chetumal, México.
Mejía-Ortíz, L.M. & Hartnoll, R.G. 2006. A new use for useless eyes in
cave crustaceans. Crustaceana, 79: 593–600.
Mejía-Ortíz, L.M. & Hartnoll, R.G. 2005. Modifications of eye structure
and integumental pigment in two cave crayfish. Jour nal of Crustacean
Biology, 25: 480–487.
Mejía-Ortíz, L.M., Hartnoll, R.G. & López-Mejía, M. 2006. Progressive
troglomorphism of ambulatory and sensory appendages in three
Mexican cave decapods. Jour nal of Natural History, 40: 255–264.
Mejía-Ortíz, L.M., López-Mejía, M., Pakes, J., Hartnoll, R.G., Zarza-
González, E. 2013. Morphological adaptations to anchialine envi-
ronments in species of five shrimp families (Barbouria yanezi, Agostocaris
bozanici, Procaris mexicana, Calliasmata nohochi and Typhlatya pearsei).
Crustaceana, 86: 578–593.
Mejía-Ortíz, L.M., Yañez, G. & López-Mejía, M. 2017. Anchialocarididae,
a new family of anchialine decapods and a new species of the genus
Agostocaris from Cozumel Island, Mexico. Crustaceana, 90: 381–398.
Paine, R.T. 1976. Size-limited predation: An observational and experi-
mental approach with the Mytilus-Pisaster interaction. Ecology, 57:
858–873.
Pérez Aranda, L. 1983. Palaemonidae Creaseria morleyi. In: Fauna de los cenotes
de Yucatán (J. Zamacona Evenes, ed.), vol. 1, pp. 1–11. Universidad
Autónoma de Yucatán, Mérida, México.
Pohlman, J.W. 2011. The biogeochemistry of anchialine caves: progress
and possibilities. Hydrobiologia, 677: 33–51.
Pohlman, J.W., Cifuentes, L.A. & Ilie, T.M. 2000. Food web dynamics
and biogeochemistry of anchialine caves: Astable isotope approach.
In: Ecosystems of the World (H. Wilkens, D. Culver & W. Humphreys,
eds.), pp. 351–363, Elsevier, Amsterdam.
Pohlman, J.W., Ilie, T.M. & Cifuentes, L.A. 1997. A stable isotope study
of organic cycling and the ecology of an anchialine cave ecosystem.
Marine Ecology Progress Series, 155: 17–27.
Downloaded from https://academic.oup.com/jcb/advance-article-abstract/doi/10.1093/jcbiol/rux098/4706304
by guest
on 10 December 2017
PREDATORY BEHAVIOR OF CAVE SHRIMP
7
Pyke, G.H., Pulliam, H.R. & Charnov, E.L. 1977. Optimal foraging:
Aselective review of theory and tests. Quarterly Review of Biology, 52:
137–154.
Schmitter-Soto, J.J., Comín, F.A., Escobar-Briones, E., Herrera-Silveira,
J., Alcocer, J., Suárez-Morales, E., Elías-Gutiérrez, M., Díaz-Arce, V.,
Marín, L.E. & Steinich, B. 2002. Hydrogeochemical and biological
characteristics of cenotes in the Yucatan Peninsula (SE Mexico).
Hydrobiologia, 467: 215–228.
Sket, B. 1996. The ecology of anchihaline caves. Trends in Ecology & Evolution,
11: 221–225.
Torres-Talamante, O., Alcocer, J., Beddows, P.A., Escobar-Briones, E.G.
& Lugo, A. 2011. The key role of the chemolimnion in meromictic
cenotes of the Yucatan Peninsula, Mexico. Hydrobiologia, 677: 107–127.
Trujillo-Pisanty, D., Chávez-Solís, E.M., Solís-Weiss, V. & Hermoso-
Salazar, M. 2010. Peracarids (Crustacea : Malacostraca) from cenote
Aerolito, Cozumel, Mexican Caribbean. Cahiers de Biologie Marine, 51:
177–180.
Vogt, G. 2012. Ageing and longevity in the Decapoda (Crustacea): Are-
view. Zoologischer Anzeiger - AJournal of Comparative Zoology, 251: 1–25.
Downloaded from https://academic.oup.com/jcb/advance-article-abstract/doi/10.1093/jcbiol/rux098/4706304
by guest
on 10 December 2017
