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Foraging and scavenging in nautilus ( Nautilus sp.) L . (Cl. Cephalopoda)

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Species of extant nautiluses (in Nautilus and Allonautilus) have been anecdotally described as opportunistic scavengers. Here, we examine foraging and scavenging behaviors of Nautilus in field and laboratory settings. Given that nautiluses are nektobenthic, solitary animals living in resource-limited habitats, we predict that odor is the predominant cue used to locate prey. Here, we show that nautiluses display a stereotyped set of search postures in the wild. In field and laboratory trials, nautiluses displayed the same stereotyped foraging postures, suggesting it is a natural and functional reflex in nautilus, and can be replicated under controlled conditions. A series of foraging behaviors induced by olfaction is a highly desirable trait to scavenge for food in the deep-sea. Considering the recent conservation initiatives and regulations now in place to protect declining nautilus populations, understanding and describing feeding behaviors and the ecology of nautiluses are a critical component to support conservation efforts.
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Foraging and scavenging in nautilus (Nautilus sp.) L. (Cl.
Cephalopoda)
Gregory J. Barord
a,b,c
, Mohammed Beydoun
b
, Spencer Bruce
d
, Virginia Li
b
,
Peter D. Ward
e
and Jennifer Basil
a,b
a
Biology Department, City University of New York – Graduate Center, New York, NY, USA;
b
Biology
Department, City University of New York - Brooklyn College, Brooklyn, NY, USA;
c
Department of Marine
Sciences, Central Campus, Des Moines, Iowa, USA;
d
Department of Biological Sciences, State University of
New York at Albany, Albany, NY, USA;
e
Biology Department, University of Washington, Seattle, WA, USA
ABSTRACT
Species of extant nautiluses (in Nautilus and Allonautilus) have been
anecdotally described as opportunistic scavengers. Here, we exam-
ine foraging and scavenging behaviors of Nautilus in eld and
laboratory settings. Given that nautiluses are nektobenthic, solitary
animals living in resource-limited habitats, we predict that odor is
the predominant cue used to locate prey. Here, we show that
nautiluses display a stereotyped set of search postures in the wild.
In eld and laboratory trials, nautiluses displayed the same stereo-
typed foraging postures, suggesting it is a natural and functional
reex in nautilus, and can be replicated under controlled condi-
tions. A series of foraging behaviors induced by olfaction is a highly
desirable trait to scavenge for food in the deep-sea. Considering the
recent conservation initiatives and regulations now in place to
protect declining nautilus populations, understanding and describ-
ing feeding behaviors and the ecology of nautiluses are a critical
component to support conservation eorts.
ARTICLE HISTORY
Received 19 May 2021
Accepted 2 November 2021
KEYWORDS
Nautilus; cephalopod;
scavenger; odor-tracking;
conservation; BRUVS
1. Introduction
A significant challenge to ethologists and conservationists is understanding how beha-
viors like foraging contribute to survival, particularly in a hard-to-observe, rare species.
The species of nautiluses are prime examples. These externally shelled cephalopods have
been described as ‘smellers and gropers’ (Saunders, 1984), but this foraging/scavenging
strategy has not been explicitly described in detail in the field or tested in the laboratory
for its ecacy to find actual food items. Here, we take a two-pronged approach to identify
the critical behaviors necessary for nautiluses, whose species are threatened by over-
fishing in the wild (Dunstan et al. 2010; 2011a; Barord et al. 2014), to detect, track, and
locate food in its dimly lit and sparse habitat. Our hypotheses and predictions are based
upon field observations by both driver and remote, deep-water videography (BRUVS, or
Baited Remote Underwater Video Systems). We subsequently test our hypotheses
CONTACT Gregory J. Barord gjbarord@gmail.com Department of Marine Sciences, Central Campus, 1800 Grand
Avenue, Des Moines, IA, USA.
Supplemental data for this article can be accessed here.
MARINE AND FRESHWATER BEHAVIOUR AND PHYSIOLOGY
2021, VOL. 54, NOS. 5–6, 241–261
https://doi.org/10.1080/10236244.2021.2003195
© 2021 Informa UK Limited, trading as Taylor & Francis Group
directly in the laboratory under controlled conditions (Synthetic Approach; Kamil 1988).
We predict that this opportunistic forager in a prey-limited, dimly lit habitat relies upon a
set of stereotyped search and swimming posture elicited by odor from a distance, to track,
locate and (sometimes) consume decaying food items.
Most cephalopod molluscs are active visual predators in the wild (see review
Boucaud-Camou and Boucher-Rodoni 1983; Castro 19913; Budelmann 1996;
Oestmann, 1997; Markaida et al., 2003; Hanlon and Messenger 2010). The coleoid
cephalopods (octopuses squid and cuttlefish) rely upon vision, camouflage, and either
eight arms (octopuses) or eight arms-two tentacles (squid and cuttlefish) to ambush their
live prey. Nautiluses (Subclass Nautiloidea) have relatively poor vision and bear up to 90
tentacles that lack suckers. Nautilus tentacles are enclosed in buccal sheaths and can
either be retracted into the sheaths (unexcited or defensive behavior) or protracted
(excited). Their tentacles are covered in taste-bud-like receptors (Ruth, 2002) and
respond to chemical cues (Basil et al. 2005). Their rhinophores (one below each eye)
detect odor at up to 10 m in the laboratory (Basil et al. 2000, 2005). Nautiluses have been
described as ‘smellers and gropers’, or scavengers, in terms of their patterns of foraging
(Saunders 1984a), swimming slowly (~5cm/s; Chamberlain 2010), searching with their
tentacles, and opportunistically feeding and scavenging on a variety of food items in their
deep-sea, dimly lit habitat (Ward and Wickstein, ; Carlson et al. 1984; Saunders 1984a;
Ward et al. 1984; Hayasaka et al., 1987). An ecologically based hypothesis (Kamil 1988)
predicts that nautiluses would detect, locate and scavenge upon food items using the
mechanism of odor tracking, as there is limited visual information available to the slow-
moving animal in its dimly lit habitat.
Odor plumes emanating from aquatic sources are slowly dissipating cues (Recent
reviews: Kamio and Derby 2017; Baker et al. 2018; Michaelis et al. 2020). These plumes
are long-lasting, particularly for decaying items; however, they are not simply a ‘con-
centration gradient’ a foraging animal can easily follow. Rather, odor is dispersed
turbulently in a patchy manner, with boluses of odor punctuated by patches of clean
water (Recent reviews: Kamio and Derby 2017; Baker et al. 2018; Michaelis et al. 2020). If
nautiluses are exploiting turbulent odor plumes to opportunistically scavenge upon
decaying food items, it would be adaptive for them to have an ecient, fast, and reflexive
response to odor cues, or more likely a series of postures that are stereotyped but respond
to changes in stimulus, like sand-digging behaviors described in Sepia ocinalis (Mather
1986). We predict the series of postures are rapidly initiated by contact with turbulent
odor cues. We test this prediction under both wild (external validity) and controlled
laboratory (internal validity) conditions.
In the laboratory, nautiluses can indeed track low-concentration turbulent odor
plumes emanating from an odor source from a distance of at least 10 m(Basil et al.
2000, 2002). Nautiluses use a combination of their rhinophores (nose, ‘smelling’) at a
distance and a specific progression of tentacles (‘groping’) in proximity to locate the
source of odor precisely (Basil et al. 2000, 2005). The cone of search is defined as a set of
behaviors described in prior studies in reaction to odor cues (cone of search, Bidder 1962;
‘smelling and groping’; Saunders 1984a). When at rest, the tentacles of nautiluses remain
retracted into the buccal sheaths and their hood is partially to fully closed. Directly after
odor washes over the animal, the hood opens, and the tentacles extend out of the buccal
sheaths (Figure 1).
242 G. J. BARORD ET AL.
Also visible at this point are the pre-ocular and post-ocular tentacles, in front of and
behind their large eyes. Far-field from the odor source, nautiluses increasingly extend
their digital and lateral tentacles outward and swim, tentacles forward, slowly and
sinusoidally in contrast to their normal mode of swimming shell forward (5 cm/s;
Chamberlain 2010). The ‘far-field’ posture is initiated by odor contact across the paired
rhinophores (‘smelling’; Saunders 1984a; Basil et al. 2000, 2005).” Far field” tentacles then
spread laterally, vertically, and dorsally, forming a ‘cone’ that expands the sensory search
area relative to the body of the animal (Bidder 1962; Boucaud-Camou and Boucher-
Rodoni 1983; Basil et al. 2000, 2005; Ruth et al. 2002). In the search area proximal to the
odor source (1 body length, Basil et al. 2000; ‘near field’), the long digital tentacles extend
downward, and drag over the substrate (‘groping’, Bidder 1962; Saunders 1984a; Basil et
al. 2000, 2005; Ruth et al. 2002; Barord 2015). Once the food item or odor source is
contacted physically by the long digital tentacles the medial tentacles then emerge to
bring the food to the mouth or to reject the item (Bidder 1962; Basil et al. 2005). Such
standardized postures in response to low concentrations of odor would be beneficial for
tracking a slow-moving odor plume emanating from a stationary source, such as a
decaying food item (Haven 1972; Ward and Wicksten,1980; Basil et al. 2000, 2005;
Ruth et al. 2002). Field observations (Barord et al. 2014) suggested that nautiluses may
even dig in the substrate for buried, decaying food items – supporting the significance of
nonvisual cues.
Figure 1. Nautilus (Nautilus pompilius) performing the cone of search’ behavior directed toward a bait
source (chicken in mesh) recorded from BRUVS along the Great Barrier Reef, Australia. Photograph
inset with close-up of nautilus showing digital tentacles (dt) and digital lateral tentacles (dlt) spread
out and hyponome (h) jetting nautilus along substrate. The wire mesh holes were 7.5cm x 9.0cm. The
nautilus is approximately 100 cm from the bait bag.
MARINE AND FRESHWATER BEHAVIOUR AND PHYSIOLOGY 243
Nautiluses throughout the South Pacific have been extensively observed via baited
remote underwater video systems, or BRUVS (Dunstan et al. 2011a; Barord et al. 2014).
These observations confirm that nautiluses are attracted to carcass bait (chicken, fish)
illuminated by a light. Here, we test the hypothesis that the foraging behaviors and cone
of search (Bidder 1962; Basil et al. 2000, 2005) documented in the laboratory is a
functional means of tracking, locating, and consuming food items in the wild as well.
We hypothesize that in the wild cone of search is also initiated far-field (presumably via
the rhinophore), whereas the digital tentacle dragging is a near-field behavior (stimula-
tion via the tentacles). We predict that in the wild, nautiluses will display the cone of
search at distances greater than one body length from the bait (Basil et al. 2000, 2005).
Distance tracking (chemotaxis, Kamio and Derby 2017; Baker et al. 2018; Michaelis et al.
2020) with the animal shifting from swimming shell-forward at a natural swimming
speed to swimming tentacles-forward slowly will follow, exhibiting the characteristics of
chemotactic tracking (Basil et al. 2000). Proximal to the source, the digital tentacles will
come into play, presumably initiated by odor contact (Basil et al. 2005). As the baited trap
in the wild also includes a visual cue, we test separately the contributions of odor and
visual stimuli to the foraging behavior in the laboratory. We predict based on prior
studies and field observations that nautiluses will rely heavily on olfactory information,
and that visual information will not play a requisite role in locating a food item.
Although nautiluses live in a deep-sea environment with minimal to no light, they may
still rely on vision to either (a) navigate their reef environment (Crook et al., 2008) or (b)
locate bioluminescent prey items, as they are positively phototactic (Muntz and Raj 1984;
Muntz 1986; Muntz, 1987). This may allow them to detect light or patterns of shadows
from great distances. Nautiluses can, for instance, use visual cues to locate and remember
a variety of white landmarks in a black maze (Crook et al. 2009, 2013; Barord 2015). We
directly tested, in the laboratory, the role of visual cues in foraging and scavenging for
food by challenging nautiluses to track and locate food items from a distance with both
visual and olfactory cues available, and with olfactory cues only – tests that are impossible
in the field. The coupling of field and laboratory study of this elusive animal is a powerful
tool to understand ecological constraints upon the behavior and conservation of nauti-
luses (Kamil 1988).
2. Materials and methods
2.1 Foraging behavior: eld trials
Food-tracking behavior
To capture the behavior of wild nautiluses, baited remote underwater video systems
(BRUVS) were deployed at four dierent geographic regions in the Indo-Pacific:
Philippines (9°35 18.87 N, 123°43 44.54 E), Australia (16°37 28.91 S, 145°53
07.35 E), Fiji 18°19 40.24 S, 178°0630.86 E), and American Samoa (14°19 19.57
S, 170°38 57.78 W) (Table 1; Barord et al. 2014). All field work was performed in
collaboration with local organizations for approval and/or permitting with University of
San Carlos (Philippines), Great Barrier Reef Marine Park Authority and University of
Queensland Animal Ethics Committee (Australia), Ministry of Fisheries (Fiji, and
Department of Marine and Wildlife Resources (American Samoa).
244 G. J. BARORD ET AL.
The BRUVS were deployed between depths of 300–400 m (fishing depth), depending
upon the local topography of the habitat where the likelihood of capturing numerous
nautiluses on film was high. At this depth, light is a limiting factor to observe nautiluses
so bright, white LED lights were used to record nautilus behavior. Each BRUVS unit
comprised one HD camcorder (Sony HDRCX440) and LED light, each enclosed in an
underwater housing unit and mounted upon a steel frame (Figure 2). A bait stick
extended from the frame in view of the camera and a rope led up to a buoy at the
surface. The BRUVS were deployed at dusk and retrieved the following dawn. Upon
retrieval, the video was downloaded to portable hard drives for later analysis of the
footage. Analysis of the footage included 1) documentation of foraging behaviors of wild
nautiluses attracted to the bait, 2) relative distance from which nautiluses are attracted to
the bait, 3) objectively defined behaviors and the distances the behaviors appeared
(including stereotyped cone of search) as well as 4) identifying potential live and dead
food items of nautiluses.
2.2 Laboratory foraging trials: husbandry
Wild-caught nautiluses from the Philippines supplied by Sea-Dwelling Creatures Inc.
were used in the laboratory studies performed at Brooklyn College Aquatic Research and
Environmental Assessment Center (AREAC), arriving in good condition. The same
nautiluses were run in both the visual/olfactory trials and the olfactory only trials.
Although nautiluses are not governed in experimental protocols, as vertebrate animals
are, laboratory care and trials were approved by the Institutional Animal Care and Use
Committee (IACUC). Maintaining nautiluses in captivity requires excellent water qual-
ity, specialized equipment, and consistent observations (Carlson, 1987; Barord and Basil
2014; Fiorito et al. 2014). Our laboratory is known for their expertise in maintaining
healthy nautiluses (Barord and Basil 2014; Barord et al. 2012; Fiorito et al. 2014). All
animals were housed in a 2625-l recirculating, artificial seawater system (Figure 3), kept
under dim 12:12 lights and at 14–17°C to simulate their deep-water natural environment.
The system included three cylindrical holding tanks (1.5 m tall, 1 m diameter), a 187.5 l
sump holding biological filtration, a mechanical pump, a chilling unit, ultraviolet filtra-
tion, and two protein skimmers supplied by two mechanical pumps. Nautiluses were
distributed in the three tanks to reduce overcrowding. Water quality and animal health
were monitored daily (pH: 7.70–8.30, Temperature: 16°C–18°C, salinity: 35 ppt, NH
3
:
0.00 mg/l, NO
2
: 0.00 mg/l, NO
3
: <15 mg/l). The water quality was within acceptable
standards for all parameters tested throughout the experiments (Carlson 1987; Barord
and Basil 2014) and weekly water changes were performed. Each animal was fed by hand
either a shrimp with shell or lobster carapace every 4–5 days. The system was cleaned and
Table 1. Data from BRUVS deployments at four survey sites (Barord et al. 2014).
Site Number of Nautiluses Number of Nautiluses Foraging Hours of Footage
Philippines 6 1 150
Australia 92 5 190
Fiji 20 3 100
American Samoa 22 4 120
MARINE AND FRESHWATER BEHAVIOUR AND PHYSIOLOGY 245
maintained daily. Animals were checked for their state of health at least two times a day.
After the trials, all nautiluses were still maintained in the laboratory and were not
euthanized.
Figure 2. Baited remote underwater video systems (BRUVS) frame deployed to record video footage of
Nautiluses at depth. The LED light (a) and HD camcorder (b) housings were fastened securely to the
mounting brackets shown above. The bait (c) was placed on the end of a ½PVC/steel stick extended
50 cm from the BRUVS frame.
Figure 3. Diagram of the aquarium system with arrows denoting water flow and color codes
corresponding to life support equipment including mechanical pumps (black boxes), chilling unit
(large gray box on right), ultraviolet filtration (gray rectangle between tank 2 and 3), and protein
skimmers (two, small gray rectangles to the right of tank 3).
246 G. J. BARORD ET AL.
2.3 Laboratory foraging trials: experimental foraging tank
The foraging tank was a rectangular (140×38×30 cm) recirculating Plexiglass aquarium
with 5 cm of sand substrate placed on the bottom (Figure 4, benthic-foraging tank). The
flow was unidirectional from upstream (point ‘U’) to downstream (point ‘D’). The
aquarium (167 l) was enclosed by a dark curtain surrounding the sides of the tank,
only allowing ambient light to come in from above. Within the curtains, two video
cameras (Panasonic HC-V720) were placed in 1) a permanent position facing the
upstream intake (camera a, Figure 4) position at the semi-random quadrant where
prey items were placed during visual/olfactory trials (camera b, Figure 4). This provided
a view upstream from the foraging animal, and a close view (camera b) of the animal at
the prey location. A TV monitor (15” COBY® LED TV1526) was connected to each video
camera so the animal could be observed from outside the curtains. The water quality
conditions of the benthic foraging tank were maintained in the same manner as the
permanent nautilus holding aquarium system. A partial water change occurred after
trials. Each nautilus (N = 10) experienced three phases during the experiment:
Sensitization, Experimental 1 (olfactory cues only), and Experimental 2 (olfactory and
visual cues).
2.4 Laboratory foraging trials, sensitization
During sensitization, each nautilus was acclimated to the benthic foraging tank for
20 minutes per day, with no shrimp present, over three days. Here, the nautiluses were
given an opportunity to freely explore the experimental tank for 20 minutes. To elicit a
positive exploratory response in the tank, a tuna slurry stimulus was created by adding
the contents of a 142 g can of tuna to 1 liter of artificial seawater and homogenizing (Basil
et al. 2000, 2005; Barord 2015). A 0.5 ml addition of the slurry was then pipetted over the
tentacles of the nautiluses at five-minute increments during the 20-min sensitization
period. The aim was to create an association to find and explore for food in the tank as in
Crook and Basil (2008). Care was taken to monitor for any stress behaviors the animals
might exhibit (hyperventilation, manifesting as ‘rocking behavior’ on the rostral/caudal
axis) in the novel tank. The animals did not exhibit any stress behaviors and swam freely
in the tank.
2.5 Laboratory foraging trials, Experiment 1: olfactory cues only
To control for visual cues and test the hypothesis that nautiluses can rely upon olfactory
cues only, one tuna-scented shrimp was buried 1 cm below the surface of the substrate,
randomly, in one of the four quadrants in the foraging tank. Cameras and monitors were
used, as in Figure 4. Each nautilus was placed in the start position and the olfactory-cue-
only trial ended when a nautilus located the buried shrimp, or when the 20 minutes
elapsed, whichever came first. Each animal was tested once per day until they successfully
found the buried prey item in three of four days (criterion). The video from each trial was
analyzed to quantify far-field and near-field swimming and tentacle postures (Bidder
1962; Basil et al. 2000, 2005; Barord 2015), path to prey, latency to find prey (learning),
and tentacle use and funnel movement at the prey location.
MARINE AND FRESHWATER BEHAVIOUR AND PHYSIOLOGY 247
2.6 Laboratory foraging trials, Experiment 2: visual and olfactory stimuli
During olfactory and visual trials, a shrimp (dipped in tuna concentrate) was placed
semi-randomly on the surface of the sand in one of four quadrants (Figure 4) down-
stream from the inlet, providing visual and odor cues to the animal’s start position further
downstream (confirmed with dye tests; as in Basil et al. 2000). Previous studies using
shrimp-infused gelatin cubes were less robust in eliciting a foraging response (Bruce
2012). The animal was then placed in the ‘start’ position and recording commenced. The
animals found that food was available in the tank, and we also documented if the animals
had to learn to find the food item, or naturally were able to track it from a distance to its
source (either visually or by using odor combined with vision in this stage of the study).
Here, the nautiluses were conditioned that food emitting visual and olfactory cues
could be found at dierent locations in the benthic foraging tank (locations that would
later become possible sites for a buried item during olfactory-only testing). Animals
(N = 10) were given three training trials, one per day, over the course of three days. Each
trial lasted 20 minutes from when the animal was placed in the ‘start’ position until food
Figure 4. Top view and side view of scavenging setup showing water flow (arrows) with the starting
position, S, in front of the intake pipe and the camera, a, facing the intake. The dotted line represents
the curtain from the top view with cameras labeled ‘a’ and ‘b’ for their positioning. Numbers 1–4
represent the quadrants within the tank that the food item was randomly placed in during each trial.
Flow was laminar in the tank from point U to point D. Arrows denote water flow in system.
248 G. J. BARORD ET AL.
was found or 20 minutes elapsed, whichever came first. The entire visual/olfactory-cue
trial was recorded, and success rates in locating the surface shrimp were calculated across
days. Criterion was met when the animal obtained the shrimp two of three days in a row.
2.7 Statistical analyses
Successfully locating the shrimp in training and testing trials was compared with non-
parametric Friedman test of dierences with repeated measures (IBM Corp, 2012). To
compare latency to find the shrimp across trials, a repeated measures ANOVA was used.
To determine if there was an overall increase in latency in testing trials, a pairwise
comparison with Bonferroni correction for multiple comparisons was used.
3 Results
3.1 Foraging behavior: eld trials
Baited remote underwater video systems (BRUVS) recorded over 400 hours of under-
water footage from the four survey sites (Table 1). A total of 148 nautiluses were recorded
via the BRUVS and 13 nautiluses were recorded exhibiting foraging behaviors (Supp.
Video 1; Supp. Video 2) directed toward visual and/or olfactory stimuli within the range
of the static camera (light and chicken/mackerel bait). The 13 nautiluses behaved in a
similar manner to those described in controlled laboratory odor-tracking studies (Basil et
al. 2000, 2005; Westermann and Beuerlein 2005). Specifically, wild nautiluses exhibited
the classic cone of search posture at a distance of greater than 5 m from the food source
(Figure 5a; Bidder 1962; Basil et al. 2000; Basil et al. 2005), extending tentacles and
swimming slowly (>5 cm/s) with tentacles forward, as opposed to swimming shell
forward as they normally do to reduce drag (Chamberlain 2010). Whether the visual
cue and/or the odor cue triggered this stereotyped behavior was unclear. All 13 of the
nautiluses displayed the cone of search behavior from a distance of at least 0.5 m to at
least 5 m from the bait source. Two nautiluses adopted the cone of search posture at least
5 m from the bait source. From 5 m, the nautiluses slowly jetted toward the bait, tentacles
first, while turning side to side (Figure 5a), as in Bidder (1962) and Basil et al. (2000);
Basil et al. (2005)). Based on these observations, the approach of nautiluses to the bait can
be described as sinusoidal and is illustrated in Figure 6.
We also documented interactions among nautiluses and potential live prey items
previously identified in the gut-contents of nautiluses (Ward and Wicksten 1980; Ward
et al. 2016). The greatest number of interactions was among the nautiluses and various
species of shrimp, presumably Heterocarpus sp. (Figure 7). One interaction was recorded
between a juvenile N. pompilius and a hermit crab (presumably Pagurus sp., Ward and
Wicksten 1980). At no point did any of the nautiluses display predatory behaviors toward
the live prey items. Instead, nautiluses directed odor-tracking and foraging behaviors
toward the dead bait only – supporting the notion they are obligate scavengers of dead
food in the wild.
MARINE AND FRESHWATER BEHAVIOUR AND PHYSIOLOGY 249
3.2 Laboratory foraging trials: sensitization
During sensitization, the nautiluses explored the entirety of the tank over the 20-min
sensitization period, often coming to rest attached to the side of the tank with their
tentacles (their most common position), and demonstrating no stress behaviors, such as
rocking back-and-forth quickly. When the tuna concentrate was pipetted over the
nautiluses’ digital tentacles, each of the nautiluses extended its tentacles outward and
jetted around the tank in exploration.
3.3 Laboratory foraging trials: Experiment 1, olfactory cues only
Search Posture: With no visual cues, and with buried shrimp only, all nautiluses initiated
the cone of search posture within 1 min of being placed in the start position. Specifically,
the hood opened, and the tentacles extended out of the buccal sheaths (Figure 8(a-b)).
Also visible at this point were the pre-ocular and post-ocular tentacles. Next, the nautilus
Figure 5. Cone of search of nautilus (Nautilus pompilius) in wild observations (a) versus laboratory trials
(b) with dierent tentacles labeled; post-ocular tentacles (pooc), pre-ocular tentacles (proc), digital
lateral tentacles (dlt), and digital tentacles (dt).
250 G. J. BARORD ET AL.
Figure 6. Representation of sinusoidal movement of nautilus (Nautilus pompilius) recorded from
baited remote underwater video systems. Movement pattern showed the nautilus jetting shell first
and moving side to side from point ‘a’ to point ‘b’ in a smaller and smaller distance. At point ‘b’ the
nautilus turned 180° and began scavenging for potential prey items with tentacles forward (b) from
point ‘b’ to point ‘c’ (as in Basil et al. 2000).
Figure 7. Nautilus (Nautilus pompilius) feeding on the bait (chicken) with several shrimps,
Heterocarpus, crawling over the nautilus. Footage from BRUVS in Panglao, Philippines (a) and Taena
Bank, American Samoa (b).
MARINE AND FRESHWATER BEHAVIOUR AND PHYSIOLOGY 251
extended its digital tentacles and lateral tentacles outward in the cone of search posture
and jetted around the tank (Figure 8c). Within 15 cm of the buried shrimp, successful
animals used a combination of digital tentacles, lateral tentacles, and exhalation jets from
the hyponome to dig/excavate in the sand substrate to search for the buried prey item
(Supp. Video 3; Figure 8d). Animals that did not ultimately excavate and/or consume the
buried shrimp also exhibited the stereotyped cone of search posture, including swimming
speed, orientation, and tentacle dragging.
During olfactory-cue-only trials, nautiluses did not improve their rates of success with
experience (learning). There were no statistically significant dierences in success rates of
locating the buried shrimp across the four trials (Friedman test; X
2
(3) = 3.581, p = .310;
latencies per trial as shown in Figure 9). Two of the nautiluses located and excavated the
shrimp on all four trials, meeting the success criterion of three of four successful trials. Of
the remaining eight nautiluses, three nautiluses located the shrimp in two out of four
trials, four nautiluses located the shrimp one out of four times, and a single nautilus did
not locate the shrimp on any attempts. Thus, 20% of the nautiluses met the success
criterion of locating and excavating the shrimp whereas 80% did not meet this criterion.
It should be noted here that the nautiluses that did not meet the criterion, still exhibited
similar foraging and scavenging behaviors during the trials. Animals found the buried
item at dierent latencies with experience (Friedman test; (X
2
(2) = 14.538, p = 0.002)),
but pairwise comparisons (SPSS, 2012) with a Bonferroni correction for multiple com-
parisons did not reveal an overall increase in latency to solve the problem across trials,
indicating learning was not a component required to find a buried food item.
3.4 Laboratory foraging trials: Experiment 2, olfactory and visual cues
Search Posture (cone of search): Prior to the 0.5 ml tuna stimulus injection, the nautiluses
remained partially to fully close in their shell with the hood closed, and their tentacles
retracted into the buccal sheaths (Figure 10a). After stimulation, nautiluses immediately
initiated the cone of search (Figure 10b), like behaviors observed in the wild (Figure 5).
During the search phase, nautiluses continued extending their tentacles and when they
came within 15 cm of the surface shrimp began to drag their digital lateral tentacles
across the substrate. Finally, when the nautilus touched the shrimp on the surface of the
substrate with one or both of its lateral tentacles, the nautilus either used its medial digital
tentacles to grab the shrimp and consume it or discard it (Figure 10(c-d) (Basil et al. 2000,
2005)).
Success rates, visual and olfactory cues: Eight of the 10 animals reached the success
criterion of locating the surface shrimp in at least two of three trials in a row. Five of the
nautiluses located the shrimp in all three trials, three found the shrimp two out of three
trials, and one located the shrimp one out of three trials. A single nautilus did not locate
or consume the shrimp on any attempts. Here, 80% of the nautiluses met the success
criterion of locating and consuming the shrimp whereas 20% of the nautiluses did not.
Again, it should be noted here that although 20% of the nautiluses did not reach the
success criterion, they still exhibit similar foraging and scavenging behaviors during the
trials. These dierences could be due to a failure to find the item, or lack of motivation
(unlikely, given the posture of the animal).
252 G. J. BARORD ET AL.
Animals did not improve in their accuracy over visual/olfactory trials as there was no
statistical dierence between successful shrimp finding across trials (Friedman test; X
2
(2) = 0.341, p = .843). Also, animals did not find the surface shrimp more quickly with
experience. There were no statistically significant dierences in latency (Figure 11) to
find the shrimp across the three visual/olfactory trials (analysis of variance with repeated
measures: F (2,18) = 3.376, p = 0.057) and no indication of learning that the visual cue
signaled a reward. Finally, the combined observations of the laboratory and field trials
can be characterized in four steps during foraging behaviors (Figure 12).
Discussion
We used a synthetic field and laboratory approach (Kamil 1988) to provide evidence
that nautiluses are obligate scavengers (Ward and Wicksten 1980) – able to detect, locate,
and even excavate distant, dead food items. Further, their scavenging strategy is not
simply a trial-and-error search but appears to be an ecient series of postures and
Figure 8. Foraging and scavenging behaviors of nautilus (Nautilus pompilius) during testing trials at
four dierent stages during buried shrimp location in the benthic arena. Pre-scent behavior char-
acterized by an overall retraction of most, if not all tentacles (a); post-scent behaviors include
extending digital tentacles (dt) and opening up of the hood to expose the post-ocular (pooc) and
pre-ocular (proc) tentacles (b); active searching for food characterized by a cone of search’ with digital
and digital lateral tentacles (dlt) extended outward with hyponome (h) propelling and possibly
excavating sediment during search (c), and finally, successful location of the prey item and subsequent
digging behaviors (d).
MARINE AND FRESHWATER BEHAVIOUR AND PHYSIOLOGY 253
tentacle behaviors in response to low concentrations of odor (cone of search) and low-
energy swimming tactics (Chamberlain 1990, 2010) that increase the likelihood of finding
food in a resource limited environment. This suite of behaviors appears to be innate, as
learning was not detected over repeated trials.
During field tests, wild nautiluses exhibited a stereotyped cone of search behavior at
least 5 m from the food source, similar to previous laboratory tests where nautiluses
detected odor plumes from over 10 m away (Basil et al. 2000), supporting the idea that
wild nautiluses may have been tracking the bait long before they entered the view of the
camera. An obvious question would be how far away the nautiluses we observed were
able to detect the food item and to eventually track and locate it. Given their extensive
horizontal and vertical migration excursions (Dunstan et al. 2011b 2011a), the distance
traveled to find a reliable food cue may be great. The cone of search and tracking
exhibited by wild nautiluses provides evidence that either (a) the nautiluses detected
the bait’s odor plume and tracked it from a distance or (b) that nautiluses are always in a
constant state of arousal for scavenging. The fact that the bait was illuminated by a light
and that nautiluses are positively phototactic may have aided in their tracking, yet they
still adopted the slow, back-and-forth tracking approach, with tentacles extended in the
cone of search, despite the bright light. It is possible that scavenging in locations with
access to food may aect their migration patterns, as the cone of search seems to be
elicited so easily.
In laboratory tests, nautiluses displayed the cone of search behavior and the series of
extensions of dierent subsets of tentacles, based upon proximity to the food item,
similar to wild nautiluses, whether the food item was visible or was buried beneath the
substrate. This supports the hypothesis that visual cues are not necessary to elicit the cone
of search and tracking behavior, and that nautiluses are likely relying upon an odor cue
(e.g. Basil et al. 2000). At distances greater than a body length from the food source, the
nautiluses moved in a larger sinusoidal curve with the shell forward and as they get closer
Figure 9. Latency of Nautilus pompilius to locate a buried shrimp across olfactory only trials. Error bars
denote SEM.
254 G. J. BARORD ET AL.
to the bait source, the series of stereotyped postures begins. This would make sense while
scavenging for prey items over great distances by (1) reducing drag and increasing jetting
eciency with shell forward and (2) by reducing predation by projecting the protective
shell forward. This too was observed in nautiluses tracking in a flume in prior studies
(Basil et al. 2000). At a certain distance, perhaps between 5 and 15 m (Basil et al. 2000),
the nautiluses turned 180° and began to move in smaller sinusoidal patterns with their
tentacles forward and in the cone of search posture. When olfactory cues signal that the
food items are close, it would benefit nautiluses to begin searching with its many tentacles
and to begin feeling along the substrate for food (‘groping’) as seen in Basil et al. (2000);
Basil et al. (2005) and in our current wild and laboratory studies. After contacting the
food item with their tentacles, nautiluses either pushed the food into its beak or discarded
it. In both cases, however, all components of the cone of search behavior were displayed
to completion during the search for the food item, whether the food was consumed
or not.
Figure 10. Foraging and scavenging behaviors of nautilus (Nautilus pompilius) during training trials
when the shrimp was placed on the surface. Pre-scent behavior characterized by an overall retraction
of most, if not all tentacles (a); post-scent behaviors include extending digital tentacles (dt) and
opening up of the hood to expose the post-ocular (pooc) and pre-ocular (proc) tentacles (b); active
searching for food characterized by a ‘cone of searchwith digital and digital lateral tentacles (dlt)
extended outward with hyponome (h) propelling and possibly disturbing sediment during search (c),
and finally, successful location of the prey item and grasping of the shrimp with its medial digital
tentacles (d).
MARINE AND FRESHWATER BEHAVIOUR AND PHYSIOLOGY 255
Figure 11. Latency of Nautilus pompilius to locate the shrimp during olfactory and visual trials when
the shrimp was placed on the surface of the substrate. Error bars denote SEM.
Figure 12. Foraging stages of nautilus (Nautilus pompilius); pre-scent (a), post-scent with preocular
(proc) and post-ocular (pooc) visible and digital tentacles (dt) being extended (b), tentacles in search
position with digital tentacles extended and digital lateral tentacles (dlt) drooping (c) and digging
with tentacles and hyponome (h) to capture prey item (d). Tentacle groups labeled as in .Ruth et al.
(2002) and Basil et al. (2005).
256 G. J. BARORD ET AL.
Here, we also showed that nautiluses may use the excurrent through their hyponome
for excavation of substrate in near-field searches. Wild and laboratory nautiluses
approached the food item along the substrate with their tentacles extended outward
and the hyponome propelling the animal along the substrate toward the location of the
food whether the food item was on the surface (olfactory cues only) or buried (olfactory
and visual cues). The hyponome therefore likely functions both in movement and
possibly for excavating the substrate, via water jets, for the buried food items the animal
has tracked. In at least 18 cases in the laboratory tests using the naturalistic, benthic
arena, we observed excavation of the buried shrimp by use of the hyponome excurrent. If
nautiluses are obligate scavengers, the dual adaptation of the hyponome for movement
and for excavating, or digging (Basil et al. 2005), may increase the likelihood of tracking
and locating of food in the near field.
However, the relatively small number of wild nautiluses exhibiting scavenging beha-
viors (13) compared to the total number of nautiluses recorded (148) was surprising. Our
criterion for wild scavenging behaviors was conservative to ensure that we were describ-
ing the same behavioral sequence between nautiluses and between field sites. An obvious
bias was the limited field of view of the video camera that was only positioned in one
direction. Potentially, nautiluses outside the initial view of the camera may have been
exhibiting the scavenging behaviors as they searched for the bait source. Of course, the
dierence in recorded behaviors may also be a result of nautiluses possessing additional
foraging/scavenging tactics during their search for food, which were not recorded in our
observations. Another possible explanation is that their positive phototactic response
overshadowed their stereotyped response to odor alone.
Although nautiluses learn and remember spatial and olfactory cues in laboratory tests
(Crook and Basil 2008; Crook et al. 2009, 2013), learning does not appear necessary for
nautiluses to track and locate food items using either olfactory cues only or olfactory and
visual cues. That nautiluses detected, tracked, and then located buried food items on the
first trial also supports the notion that this is a strongly innate behavior in response to
odor. Further, this stereotyped behavior continued to completion even when the nautilus
rejected the food item. Such a stereotyped search sequence, elicited easily and from a
distance, would suit an animal that is primarily an opportunistic feeder in an unpredict-
able environment.
Individual dierences in appetite or preferred food item may have been responsible
for the inconsistent success rates of nautiluses locating the food item in the benthic
foraging arena. While husbandry conditions for nautiluses have been significantly
improved (Carlson 1987; Barord and Basil 2014; Fiorito et al. 2014), the diet of captive
(and wild) nautiluses is still not well known. Understanding the exact ‘hunger level’ of a
nautilus is therefore extremely dicult. Perhaps, the nautiluses in the benthic arena were
not motivated to consume the prey item because they were simply not hungry. However,
whether they consumed the food item or not, both wild and laboratory nautiluses
displayed the stereotyped cone of search at a distance from food, and near-field tentacle
behavior proximal to the item, even buried, again underscoring that it may be an innate
behavior whether they are hungry or not. Lack of motivation was unlikely given the
robust posture of the animal. Although we did observe similar behaviors of nautiluses in
MARINE AND FRESHWATER BEHAVIOUR AND PHYSIOLOGY 257
the field and laboratory, even with dierent food types oered, this dierence could have
impacted our results. Future fieldwork should incorporate more natural food items that
the nautiluses would encounter in their ecosystems.
From detecting the odor to excavating the food item, this stereotyped sequence of
directed behaviors is an ecient means to locate even hidden food items by an oppor-
tunistic scavenger. Stationary decaying or buried food items emit a more stable and long-
lasting odor plume on a timescale that the slow-moving nautilus can exploit, when
compared to living and moving prey items. Wild nautiluses in fact fed on the dead-
food source even though they were close to, or covered by, living prey items, such as
shrimp and hermit crabs – all prey items naturally found in the gut contents of wild
nautiluses (Ward and Wicksten 1980). In no case did wild nautiluses direct the foraging
behaviors toward the live prey. Future controlled laboratory tests giving animals choices
between live and dead prey will test our field-based ‘obligate-scavenger hypotheses’ more
directly.
While a stereotyped and robust response to low doses of odor is an ecient means for
an opportunistic forager to find food, there are also potential risks associated with this
mode of feeding. Nautilus populations are in decline in the wild (DeAngelis 2012; Barord
et al. 2014) due to overfishing for their shells. All nautiluses (Family Nautilidae) were, as a
consequence, listed in Appendix 2 of the Convention on International Trade in
Endangered Species (CITES) in 2017. The primary mode of fishing is by using traps
baited with some type of dead food item, such as chicken, tuna, and mackerel. Given the
strength and ecacy of the sequence of postures to track odor cues, such traps can and do
attract high numbers of nautiluses, likely from a great distance (Barord et al. 2014),
leading to rapid depletion of local populations. As nautiluses are late to mature, slow to
breed, and do not migrate across open water, local populations have been reduced
drastically – with little chance for recovery (DeAngelis 2012; Barord et al. 2014). Thus,
‘fishing’ for nautiluses has more accurately been described as ‘mining’ without replace-
ment by researchers in the field (Dunstan, personal communication).
Specific components of the foraging behaviors may also have additional negative
implications for their status in the wild. As nautiluses dig for prey items in the substrate,
they may be exposed to toxins that have settled on and within the sediment because of
increasing coastal development and sedimentation (Rainbow 1997; Kraepiel et al. 2003;
Hammerschmidt and Fitzgerald 2006; Squadrone et al. 2013; Gworek et al. 2016; Peter et
al. 2018). Even more, the microvillus epidermis of nautiluses, and all cephalopods, results
in a greater uptake of potential toxins in the water. The rate and impact of processes such
as sedimentation in nautilus habitat are unknown. Thus, future studies using core and
water-column samplers would provide data on the impact that anthropogenic sources are
having on nautilus habitat and populations. By continuing to address questions of the
natural history of these deep-sea, solitary animals using an integrative approach, we can
answer critical questions regarding the natural ecology of nautilus to support conserva-
tion eorts.
258 G. J. BARORD ET AL.
Acknowledgments
The authors would like to thank the lab members of the Laboratory for Invertebrate Behavior and
Ecology for assistance in maintenance and husbandry of the nautiluses. Rob Dickie and the
Aquatic Research and Environmental Assessment Center also provided husbandry support during
the project. Frank Grasso and Heike Neumeister provided helpful insight in the design and
experimental trials.
Disclosure statement
The authors declare that there are no relevant financial or non-financial competing interests to
report.
Data Availability Statement
The video data that support the findings of this study are available from the corresponding author
(GJB) upon request.
Funding
This work was supported by the Binational Israel/USA Foundation, PSC-CUNY, the United States
Fish and Wildlife Service (#10170-J-001), the Tiany Foundation (#11661), the National Science
Foundation (NSF GDE-0638718), the Norman M. Saks Travel Award, The Minnesota Zoo Ulysses
S. Seal Conservation Grant, the Riverbanks Zoo and Garden Conservation Award, the National
Oceanic and Atmospheric Administration (NA11NMF4720256), and the Phoenix Zoo
Conservation Award;PSC CUNY;United States-Israel Binational Science Foundation;
ORCID
Gregory J. Barord http://orcid.org/0000-0002-4482-8016
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... This Triassic morphology is very similar to that of modern rhyncholites (especially those in Nautilus macromphalus). Modern nautiluses are considered opportunistic carnivores and have a durophagous diet, as they have been observed feeding on crustaceans, crabs, and lobsters, but also carrion (Ward & Wickstein 1980;Saunders & Ward 2010;Barord et al. 2021). Triassic nautilids probably showed a similar diet (Klug 2001). ...
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Here, we investigate three aspects of nautilus life history as it relates to conservation by combining laboratory and field studies: navigational tactics, feeding behaviors, and population demography. Nautiluses learn and remember visual cues to find a goal using a beacon, or constellation of cues around the goal. However, the contribution of kinesthetic, or route memory, as they navigate to the goal, is unknown. Here, we tested the nautiluses’ ability to navigate a maze by shifting or removing a visual beacon cue used to identify the goal. We found that after learning that a beacon cued a goal in a spatial maze, nautiluses switched to route memory to find the goal when the beacon was removed. However, this switch was difficult for them. Nautiluses tested with a shifted beacon, 45° relative to the goal, ignored their route memory to orient toward the beacon instead. 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Effective conservation plans benefit both the species of interest as well as the community. We identify visual and kinesthetic cues and tactics that are important to nautiluses returning to locations in their habitat (e.g., hiding spots, good foraging), and support the hypothesis that nautiluses are strict scavengers, sometimes reliant on digging in the substrate to find food they have found using olfactory cues. We also report on the health of populations in both fished and unfished sites in the Indo Pacific. There is still work to perform, such as identifying preferred habitat type, preferred species of prey, and calculating abundance levels at different areas and at different times. However, without protection, fisheries will continue to deplete nautiluses to extinction, one population at a time, as the fishermen move to new sites when one site is no longer profitable.
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