Download Habitat location and selection by the Sargassum crab Portunus sayi

HABITAT LOCATION AND SELECTION BY THE SARGASSUM CRAB
PORTUNUS SAYI: THE ROLE OF SENSORY CUES
by
Lorin E. West
A Thesis Submitted to the Faculty of
The Charles E. Schmidt College of Science
in Partial Fulfillment of the Requirements for the Degree of
Master of Science
Florida Atlantic University
Boca Raton, Florida
August 2012
Copyright by Lorin E. West 2012
ii ACKNOWLEDGEMENTS
First and foremost, I would like to thank my advisor Dr. Randy Brooks for his
guidance and supervision throughout my graduate career and for his time spent
sacrificing his boat, which made collecting samples in the field possible. Special thanks
go to Dr. Brian Lapointe for taking me under his wing as if I were one of his own
graduate students and for providing me with amazing research opportunities. I would also
like to thank the rest of my committee members, Dr. Tamara Frank and Dr. Dennis
Hanisak, for agreeing to be on my committee despite their busy schedules and for their
direction throughout the development of my thesis. Thanks to my labmates, Chelsea
Bennice and Ed Davis, for their help with sampling and making late hours in the lab
much more tolerable.
iv ABSTRACT
Author:
Lorin E. West
Title:
Habitat Location and Selection by the Sargassum Crab Portunus
sayi: The Role of Sensory Cues
Institution:
Florida Atlantic University
Thesis Advisor:
Dr. W. Randy Brooks
Degree:
Master of Science
Year:
2012
The Sargassum community consists of a unique and diverse assemblage of fauna
critical to pelagic food chains. Associated organisms presumably have adaptations to
assist in finding Sargassum. This study investigated cues used for habitat location and
selection by the Sargassum crab, Portunus sayi. Chemical detection trials were conducted
with a two-chamber choice apparatus with Sargassum spp. and Thalassia testudinum as
source odors. Visual detection trials (devoid of chemical cues) and habitat selection trials
were conducted in which crabs were given a choice between habitats. Results showed
that P. sayi responded to chemical odors from Sargassum spp. Crabs visually located
habitats but did not visually distinguish between different habitats. In habitat selection
trials, crabs selected Sargassum spp. over artificial Sargassum and T. testudinum. These
results suggest that crabs isolated from Sargassum likely use chemoreception from longer
distances; within visual proximity of a potential patch, crabs use both chemical and visual
information. v HABITAT LOCATION AND SELECTION BY THE SARGASSUM CRAB
PORTUNUS SAYI: THE ROLE OF SENSORY CUES
List of Tables ................................................................................................................... viii List of Figures .................................................................................................................... ix Introduction ......................................................................................................................... 1 Chemoreception in decapods ........................................................................................ 4 Visual reception in decapods ........................................................................................ 6 Objectives ..................................................................................................................... 8 Methods............................................................................................................................... 9 Collection and maintenance of specimens .................................................................... 9 Chemoreception experiments...................................................................................... 10 Visual reception experiments ...................................................................................... 12
Habitat selection experiments ..................................................................................... 13
Statistical analysis ....................................................................................................... 14
Results ............................................................................................................................... 15
Chemoreception experiments...................................................................................... 15 Visual reception experiments ...................................................................................... 15 Habitat selection experiments ..................................................................................... 16 Discussion ......................................................................................................................... 18 Chemoreception experiments...................................................................................... 18 Visual reception experiments ...................................................................................... 20 vi Habitat selection experiments ..................................................................................... 21
Conclusions ................................................................................................................. 23
Appendixes ....................................................................................................................... 25 References ......................................................................................................................... 39
vii TABLES
Table 1. Fisher’s Exact and logistic regression results for chemoreception trials. ........... 25
Table 2. Binomial test results for visual reception trials .................................................. 26 Table 3. Fisher’s Exact and logistic regression results for visual reception trials ............ 27
Table 4. Fisher’s Exact and logistic regression results for visual reception controls ....... 28 Table 5. Fisher’s Exact and logistic regression results for habitat selection trials ........... 29 Table 6. Fisher’s Exact and logistic regression results for habitat selection controls ...... 30 viii FIGURES
Figure 1. Chemoreception experimental apparatus .......................................................... 31
Figure 2. Visual reception diagram................................................................................... 32
Figure 3. Habitat selection diagram. ................................................................................. 33
Figure 4. Chemoreception graph....................................................................................... 34
Figure 5. Visual reception graph ....................................................................................... 35 Figure 6. Visual reception control graph .......................................................................... 36 Figure 7. Habitat selection graph ...................................................................................... 37 Figure 8. Habitat selection control graph .......................................................................... 38 ix INTRODUCTION
Pelagic Sargassum is a brown alga characterized by numerous blades, a highly
branched thallus, and air bladders called pneumatocysts, which creates a unique floating
habitat common throughout the western North Atlantic Ocean and the Gulf of Mexico
(Parr, 1939). Most of these pelagic mats are comprised of two species, Sargassum
fluitans Børgesen and Sargassum natans (Linnaeus) Gaillon (Parr, 1939). The
distribution of both species of Sargassum is highly variable in space and time, and
influenced by currents, gyres (such as the North Atlantic Central Gyre), eddies, and
winds (Wells and Rooker, 2004). These Sargassum communities, or “weedlines,”
accumulate at the surface as a result of windrows from Langmuir circulation (Ryther,
1956) and support a diverse assemblage of invertebrates, fish, sea turtles, pelagic birds,
and marine mammals (Butler et al. 1983; Casazza and Ross, 2008).
Habitat utilization begins with early colonizers such as bacteria, hydroids, and
bryozoans that start ecological succession to provide the base of the Sargassum
community food chain (Dooley 1972). There are approximately 100 species of sessile
and motile invertebrates within this community, of which many are endemic (Butler et al.
1983). One of the major groups of invertebrates within Sargassum is decapod crustaceans
(Butler et al., 1983). Specifically, the Sargassum crab, Portunus sayi, is one of the most
frequently observed associates within Sargassum mats. Like many of these
1
endemic invertebrates, P. sayi has adapted to life within the Sargassum community and
displays coloration patterns mimicking the appearance of Sargassum stipes and blades for
camouflage (Dooley, 1972).
Sargassum and the array of invertebrates in this community serve as shelter and
prey for more than 100 fish species (Wells and Rooker, 2004; Casazza and Ross, 2008).
These species of fish range from obligatory, like the endemic Sargassum fish (Histrio
histrio) and the Sargassum pipefish (Sygnathus pelagicus) with morphological
adaptations for life in Sargassum, to facultative relationships (Wells and Rooker, 2004).
For pelagic fish species, many of which are commercially and recreationally important
(e.g., dolphinfish, tuna, ballyhoo, jacks, sailfish, swordfish, and marlin), Sargassum mats
serve as a nursery for juvenile fish (Dooley, 1972; Costen-Clements, 1991; Wells and
Rooker, 2004; Rudershausen et al., 2010). As a result, Sargassum mats are designated as
Essential Fish Habitat (EFH) by the National Marine Fisheries Service (NMFS) (NOAA,
1996). Sargassum also provides habitat for four of the seven sea turtle species (Carr,
1987; Manzella and Williams, 1991) and 23 seabirds species (Haney, 1986).
The first documentation of Sargassum mats can be traced back to Columbus’
journal written in 1492 (Dunn and Kelly, 1989). Since then much research has been
conducted on the fauna associated with Sargassum and habitat use by fish species (Parr,
1939; Weis, 1968; Dooley, 1972; Ryland, 1974; Butler et al., 1983; Stoner and Greening,
1984; Kingsford and Choat, 1985; Wells and Rooker, 2004; Casazza and Ross, 2008).
However, little work has been done on the ecological and biological interactions of
inhabitants within Sargassum communities (Johnson and Atema, 1986; Brooks et al.,
2007; Jobe and Brooks, 2009). The numerous associated invertebrate and vertebrate
2 fauna of Sargassum mats offer potentially dynamic research discovery opportunities. The
Sargassum crab, P. sayi, is one of the more ubiquitous, macroscopic faunal inhabitants in
these mats and was chosen as the focus of this study.
Faunal diversity (including crab presence) is typically high, while the spatial
presence of Sargassum is temporally and spatially variable. For example, seasonal
variation in Sargassum abundance exists (Stoner, 1983) and physical factors influence
Sargassum distribution (Wells and Rooker, 2004). Lapointe (1986, 1995) showed that
primary productivity of Sargassum is much greater in neritic than oceanic waters, due to
increased nitrogen and phosphorus availability. This variation in the abundance and
presence of Sargassum mats raises the question on how recruitment of organisms occurs.
Both juveniles and those individuals separated from mats by biotic events [e.g., feeding
by large, pelagic species like dolphinfish (Dooley, 1972; Costen-Clements, 1991; Wells
and Rooker, 2004; Rudershausen et al., 2010)], and abiotic events (e.g., wind and waves
that break up patch sizes, or when mats are driven onto beaches) must locate a new mat.
What cues might P. sayi and other motile inhabitants use for such relocation? Visual
cues, in the daytime, would be available at certain distances. However, chemical cues
would potentially be available at all times, and distance would be less of a problem than
using visual cues exclusively. Molecules released by Sargassum spp. could potentially be
detected in the water column (Hanson, 1977; Arnold and Targett, 2000; Wong and
Cheung, 2001; Turner and Rooker, 2006; van Ginneken et al., 2011).
The seagrass, Thalassia testudinum, has been observed floating inshore and
washed up on shore intermixed within patches of Sargassum. When Sargassum washes
on shore, the associated fauna is highly susceptible to desiccation and predation and will
3 likely abandon the current mats. Although P. sayi has morphological adaptations for
living within the Sargassum community, it is feasible that these crabs may be generalists
and select more than one habitat (such as T. testudinum) if given a choice. Two other
crustacean Sargassum associates, the shrimps Leander tenuicornis and Latreutes
fucorum, are known to inhabit T. testudinum in benthic, coastal regions (Bauer, 1985;
Leber, 1985). Thus, this seagrass serves as an alternative habitat for some of the
Sargassum decapod inhabitants.
Chemoreception in decapods
Chemical cues are a specific type of sensory cue involving the detection of
molecules. Within the marine environment, molecules released by organisms disperse
and can induce a behavioral response in organisms that perceive the signals (Zimmer and
Butman, 2000). Decapod crustaceans can detect numerous waterborne compounds,
including amino acids, amines, ammonium, hydrocarbons, nucleotides, peptides,
proteins, sugars, and fatty acids (Rittschof, 1992; Markowska et al., 2008). Chemical
signaling processes play an important role in marine ecological interactions. For example,
sensory perception of chemical cues in decapods influence mate and symbiont detection,
habitat identification and selection, metamorphosis, predator avoidance, prey location,
and conspecific communication (Gleeson, 1980; Brooks, 1991; Zimmer and Butman,
2000; Krimsky and Epifanio, 2008; Anderson and Epifanio, 2010).
Chemical signaling used by decapods is important for mating behavior and mate
selection (Dunham, 1978). Gleeson (1980) showed that when pubescent blue crab
females release hormones, males display specific courtship behavior. Aquiloni et al.
4 (2009) found that male crayfish rely solely on olfactory cues to locate female
conspecifics, while females use chemical and visual stimuli to locate and select male
mates. Brooks (1991) showed that chemical cues can also be used for symbiont detection,
in which the hermit crab, Dardanus venosus, chemically detected its symbiotic sea
anemone, Calliactis tricolor. Brooks and Rittschof (1995) also showed that the
porcellanid crab, Porcellana sayana, was chemically attracted to its symbiont, C.
tricolor.
Habitat identification is a primary cue for metamorphosis of decapod larvae and
important for decapod distribution. Forward et al. (2003) found that megalopae of the
blue crab, Callinectes sapidus, respond to chemical cues from aquatic vegetation by
orienting toward these areas. Krimsky and Epifanio (2008) also found that there was a
significant effect on stone crab metamorphosis times when crabs were exposed to cues
associated with S. fluitans, indicating that juvenile stone crabs use Sargassum mats as a
possible nursery habitat. In addition, Lecchini et al. (2010) showed that xanthid crabs
selected sand over macroalgae using chemical cues.
Conspecific location is also an important chemical cue for decapod larva
metamorphosis. A study with the Asian shore crab, Hemigrapsus sanguineus, showed
that there was a higher percentage of megalopae undergoing metamorphosis when adult
crabs were present, indicating that megalopae can chemically detect conspecific adults
(Anderson and Epifanio, 2010). Another study by Gebauer et al. (1998) showed that
chemical detection of adult conspecific odors by megalopae of the Atlantic burrowing
crab, Chasmagnathus granulate, reduced the time until metamorphosis.
5 Chemical detection of predators by decapods can also affect decapod distribution
and abundance. Crowl and Covich (1994) showed that the distribution of freshwater
shrimp within a stream is determined by the presence of chemical cues from a larger
predatory shrimp. Forward et al. (2003) found that the blue crab reverses its orientation
when chemical cues from predators are detected. Another study by Brooks (1991)
showed that the hermit crabs, Dardanus venosus and Pagurus pollicaris, strongly
avoided chemical cues from a predatory octopus.
Chemical cues can alter the outcome of foraging by decapods responding to prey
odors. Foraging behavior of the blue crab, C. sapidus, is affected by chemical cues from
clam and oyster mantle fluid and chemicals from wounded prey (Finelli et al. 2000).
When these cues are detected, C. sapidus begins to search and eventually move in the
general direction of the chemical source.
Visual reception in decapods
Arthropods, including decapod crustaceans, are unique in that they possess
moveable, stalked compound eyes, permitting broader fields of view and an increased
binocular spread (Cronin, 1986). Marine crustaceans that inhabit different light
environments throughout their life-history require sensory changes and almost always
metamorphose from a planktonic larval stage into either a benthic or nektonic adult stage
(Cronin and Jinks, 2001). Even when the light environment of the larval and adult stage
of crustaceans is the same, the visual system of the adults is still more complex than that
of the larvae (Cronin and Jinks, 2001).
6 The primary functions of decapod larval vision include: orientation in the water
column, vertical migration, and avoidance of predators (Forward, 1976, 1977; Forward et
al., 1984; Cronin, 1986; Cronin and Jinks, 2001). Forward et al. (1984) showed that
vertical migration of the estuarine crab, Rhithropanopeus harrisii, results from a
photoresponse to light levels during the day. Other studies by Forward (1976, 1977)
showed that larval crabs use vision to avoid predation by photonegative swimming when
there was a decrease in light intensity. The behavior to this light intensity decrease has
been termed the “shadow response” and occurs at dusk or when a predator passes by
(Forward, 1976, 1977).
In addition to the functions of decapod larval vision, adult decapods use vision for
navigation and orientation, prey recognition and capture, habitat selection, mate selection,
and communication (Cronin, 1986; Vannini, 1987; Diaz et al., 1995; Cronin and Jinks,
2001; Detto, 2007). The pebble crab, Eriphia smithi, uses visual cues to relocate holes
within a cliff after foraging, as blinded crabs took spiral paths and eventually stopped
walking until submerged by the high tide (Vannini, 1987). Habitat selection based on
vision is demonstrated by the hermit crab, Clibanarius vittatus, which visually
discriminates between shells of different species for its home (Diaz et al., 1995). Detto
(2007) documented the use of vision for mate selection in the female fiddler crab, Uca
mjoebergi, in which the females use color vision to detect claw coloration for recognition
of male conspecifics. Similarly, male fiddler crabs and male semaphore crabs exhibit a
claw wave as a means of visual communication with conspecifics (Pope, 2000; Kitaura
and Wada, 2006, respectively). Visual cues for predator avoidance have been observed
7 for the blue crab, C. sapidus, which engages in rapid movements in the offshore
direction when presented with an image of a predator (Woodbury, 1986).
Objectives
In this laboratory study, the following questions related to habitat location and
selection by the Sargassum crab, P sayi, were addressed:
1.
Does P. sayi respond to chemical cues from S. fluitans, S. natans, and T.
testudinum?
2.
Does P. sayi respond to visual cues from S. fluitans, S. natans, and T.
testudinum?
3.
Does P. sayi exhibit habitat selection differences between S. fluitans, S.
natans, artificial Sargassum, and T. testudinum?
8 METHODS
Collection and maintenance of specimens
All specimens were collected via boat 4-12 km offshore from the Boca Raton
Inlet in southeast Florida from April 2011 through September 2011. S. natans, S. fluitans,
T. testudinum, and P. sayi were collected from the surface of Sargassum mats with a fine
mesh dip net. All specimens were quickly sorted on the boat and specimens not used for
experiments were released back into the Atlantic Ocean. All Sargassum, Sargassum
crabs, and T. testudinum required for experimentation were transported in StyrofoamTM
containers with portable aerators to the laboratory in the Biological Sciences building at
Florida Atlantic University.
In the laboratory, Sargassum species and T. testudinum were separated and placed
in aquaria. Sargassum crabs were placed in individual aquaria and acclimated for 24 h
prior to experimental trials. All aquaria were set up with seawater obtained from Gumbo
Limbo Nature Center in Boca Raton Florida, where saltwater is pumped directly from the
Atlantic Ocean. Salinity within all aquaria remained between 32-35 ppt and specimens
were exposed to a 12L:12D photoperiod. All crabs were fed brine shrimp daily.
Crab size was determined by measuring the carapace width. However, juvenile
and adult categories were not assigned (due to lack of literature on the life history of P.
sayi). Preliminary observations showed that crabs collected varied in size from 2-41 mm.
Crabs tested were > 5 mm, as smaller crabs were too difficult to handle without causing
9 potential injury. Individual crab sex was distinguished by morphological differences in
males vs. females (Feldmann, 1998) and equal numbers of male and female crabs were
used for all experiments.
Chemoreception experiments
Chemoreception experiments were conducted in a test apparatus adapted from
Wass and Colgan (1992) and consisted of four tanks with gravity fed seawater flow
(Figure 1). The two top “stimulus” tanks (41x20x25 cm high) fed water through plastic
tubes (6 mm in diameter) into the lower “choice” tank (41x20x25 cm high) at a rate of 10
ml per minute (Reeves and Brooks, 2001). One “stimulus” tank contained seawater with
chemical cues, while the second “stimulus” tank contained only seawater. Both
“stimulus” tanks were out of view from P. sayi, to eliminate visual cues.
The “choice” tank contained two opaque partitions sealed to the bottom and the
back side of the tank, to create three semi-enclosed compartments. Each side
compartment had an 8-cm wide opening for the crabs to pass through from the center
compartment. A second pair of outflow tubes (secured along the backside of the center
compartment) allowed seawater to flow at a rate of 10 ml per minute into a fourth
“collection” tank placed below the “choice” tank. All positioning of tubing was measured
and placed at equal distances to ensure that flow patterns within each compartment were
identical. Two different colored dyes were used before experiments to color seawater
(one for each “stimulus” tank) to verify that the flow patterns were identical within both
side compartments and that there was minimal mixing in the central compartment.
10 During each trial, tubing from the “stimulus” tank released seawater containing
one of the three chemical cue sources: 1) S. natans, 2) S. fluitans, and 3) T. testudinum,
into one side of the “choice” tank. The other “stimulus” tank contained and released
seawater devoid of chemical cues into the other side of the “choice” tank. The chemical
cue “stimulus” source was in the form of a clump weighing 30 + 0.1 g adapted from Jobe
and Brooks (2009). Clumps of Sargassum spp. and T. testudinum were used only once to
establish odor water for the “stimulus” tank. Prior to the start of each trial the clump was
randomly placed in one “stimulus” tank and after 20 minutes all tubing was unclamped.
After 60 seconds, one crab was placed in front of the outflow tubes in the center
compartment with a dip-net. The observer recorded the following data: 1) activity and
movements of the crab; 2) the compartment that the crab first entered; 3) elapsed time
before the crab left the central compartment. Tests ended when the crab chose a side
compartment by leaving the central compartment and crossing the partition (adapted from
Waas and Colgan, 1992).
Preliminary trials showed that the majority of crabs chose a side compartment
within the first 5 minutes and remained there (n = 20). Therefore, trials lasted no longer
than 30 min. At the end of each trial, all tanks and tubing were emptied and rinsed to
remove potential lingering odors before the beginning of the next trial. Twenty replicates
were conducted for each of the experimental variables and each individual crab was used
only once for one treatment. Trials were also conducted to determine if P. sayi could
chemically distinguish between both species of Sargassum simultaneously. Thus, instead
of keeping one “stimulus” tank devoid of chemical cues, S. fluitans was in one “stimulus”
tank while S. natans was in the other one. Controls in which both “stimulus” tanks
11 contained seawater were conducted to determine how crabs responded in the absence of
chemical cues. The sizes of crabs ranged from 7.0-36.7 mm and weighed between 0.0874.711 g.
Visual reception experiments
Experiments were conducted to determine if visual cues are used by P. sayi for
habitat location and selection. Each crab was placed individually in aquaria with a choice
between two habitats, each of which was placed inside a clear plastic container (9x16x11
cm high) (Figure 2). Each container was placed at opposite ends within aquaria
(41x20x25 cm high). The specific visual reception treatments conducted were as follows:
1) S. fluitans vs. S. natans; 2) S. fluitans vs. artificial Sargassum (a plastic mimic custom
made by Bio Models Co. used to display the visual features of Sargassum); 3) S. natans
vs. artificial Sargassum; 4) S. fluitans vs. T. testudinum; 5) S. natans vs. T. testudinum.
Control tests were also conducted to determine the response of crabs in the presence of
only one habitat (e.g., one clear container was empty), which included the following
trials: 1) S. fluitans vs. control; 2) S. natans vs. control; 3) artificial Sargassum vs.
control; 4) T. testudinum vs. control. Preliminary trials showed that crabs had no zone
preferences within aquaria when both containers were empty (n = 20). Each clump of
Sargassum (live and artificial) and T. testudinum was 9x16x7 cm within its respective
container and weighed 30 + 0.1 g. P. sayi was placed in the center of the tank after the
two habitat patches were arranged within the plastic containers. To avoid interference of
chemical and tactile cues, the opening of the plastic containers remained above the water
level in the aquarium.
12 For recording purposes, the aquaria were visually divided into three zones by
drawing lines on the upper rim of the aquarium not visible to the crab (adapted from Jobe
and Brooks, 2009). The visual selection of the crab was recorded based on the zone in
which the crab was located after a 2 h trial. Preliminary trials showed that crabs might
switch back and forth between habitats for about 30 min before choosing and remaining
in a habitat zone (n = 20). Therefore, the crab’s location within the aquaria was
monitored and recorded initially and every 30 min. Crab sizes ranged from 6.0-39.0 mm
and weights ranged from 0.085-4.711 g.
Habitat selection experiments
Experiments were conducted for habitat selection by P. sayi. Each crab was
placed in aquaria individually with the option of choosing one of the two habitats
provided. Habitat selection treatments conducted were as follows: 1) S. fluitans vs. S.
natans; 2) S. fluitans vs. artificial Sargassum; 3) S. natans vs. artificial Sargassum; 4) S.
fluitans vs. T. testudinum; 5) S. natans vs. T. testudinum. The two patches of habitat were
placed in aquaria (41x20x25 cm high) floating at opposite ends. Patches of Sargassum
(live and artificial) and T. testudinum were spread out to be approximately 11x16x6 cm
and weighed 30 + 0.1 g. Despite morphological differences between the more robust
Sargassum spp. and the flat blades of T. testudinum (and using the same weight), similar
habitat size was achieved by arranging the blades in various three dimensional directions
as they would be found naturally, instead of flat on top of one another. Similar to the
visual cues trials, aquaria were visually divided into three zones by drawing lines on the
top of the aquarium rim (Figure 3). Once the two habitat patches were arranged, each trial
13 began with the placement of one crab in the center of zone 2 in the aquarium. Habitat
selection was recorded based on the zone in which the crab was located after the 2-hr
trial. The crab’s location within the aquarium was monitored and recorded initially and
every 30 min.
Control trials were conducted to determine the response of crabs when only one
habitat was available (e.g., one side of the aquaria was empty) and included the following
trials: 1) S. fluitans vs. control; 2) S. natans vs. control; 3) artificial Sargassum vs.
control; 4) T. testudinum vs. control. Preliminary trials were conducted in which all zones
were empty to show that there were no zone preferences within aquaria (n = 20). The
sizes of crabs used for habitat selection trials ranged from 6.0-33.0 mm and weights
ranged from 0.021-4.027 g.
Statistical analysis
Each crab was used only once for one trial in one treatment and a total of 20
replicates were conducted for each treatment for all experiments. Results from all
experiments were analyzed using the binomial (Z) test of significance by comparing the
number of crabs in each compartment/zone to the expected probability of 50% (Brooks
and Rittschof, 1995; Reeves and Brooks, 2001; Jobe and Brooks, 2009). Fisher’s Exact
test was used to determine any differences in selections between males and females. To
determine effects of size and weight on selections made by P. sayi, a logistic regression
was used.
14 RESULTS
Chemoreception experiments
P. sayi showed a significant ability to respond to chemical odors in two of the
three chemoreception trials (Figure 4). P. sayi chose S. fluitans odors more than the
control odors (17 out of 20 or 85%; Z = 3.131; P = 0.002) and S. natans odors more than
the control (16 out of 20 or 80%; Z = 2.683; P = 0.007). The difference between T.
testudinum odors and the control selection was not significant; however, numerically the
control was chosen more by P. sayi than the T. testudinum odor (14 out of 20 or 70%; Z =
1.789; P = 0.07). P. sayi had no significant preference for S. fluitans vs. S. natans odors
(13 vs. 7; Z = 1.342; P = 0.18). The results from the control trials also showed no
significant difference between the right and left choice chambers (11 vs. 9; Z = 0.447; P
= 0.65). There was no significant difference in selection between male and female crabs
for all chemoreception trials (Table 1; Fisher’s Exact test, P > 0.05). Size and weight of
P. sayi had no significant effect on any chemical odor selections (Table 1; Logistic
regression, P > 0.05 for both).
Visual reception experiments
P. sayi did not significantly choose between different habitats for any of the five
visual reception treatments (P > 0.05, Table 2, Figure 5). Although the resulting trials
were not significant, the initial habitat selections between S. natans and T. testudinum by
15 P. sayi were significantly different. P. sayi initially chose S. natans significantly more
than T. testudinum (15 out of 20 or 75%; Z = 2.236; P = 0.025) and although not
significant, S. fluitans was initially chosen more than T. testudinum (14 out of 20 or 70%)
when the trials first began. There was no significant difference between male and female
choices for visual selection trials (Table 3; Fisher’s Exact test, P > 0.05). The size and
weights of P. sayi had no significant effect on choices for visual selection trials (Table 3;
Logistic regression, P > 0.05).
Control trials showed that P. sayi significantly selected containers with habitats
over empty containers for all four treatments (Figure 6). Specifically, P. sayi chose S.
fluitans more than the control ( 15 out of 20 or 75%; Z = 2.236; P = 0.025), S. natans
more than the control (16 out of 20 or 80%; Z = 2.683; P = 0.007), T. testudinum more
than the control (16 out of 20 or 80%; Z = 2.683; P = 0.007), and artificial Sargassum
more than the control (17 out of 20 or 85%; Z = 3.131; P = 0.002). There were no
significant differences in choices between male and female crabs or between size and
weight for the visual location trials (Table 4; Fisher’s Exact test, P > 0.05; Logistic
regression, P > 0.05 for both size and weight).
Habitat selection experiments
P. sayi had significant habitat selections in four of the five habitat pairings (Figure
7). P. sayi chose S. fluitans more than artificial Sargassum (18 out of 20 or 90%; Z =
3.578; P < 0.001) and S. natans more than artificial Sargassum (16 out of 20 or 80%; Z =
2.683; P = 0.007). Differences in responses between both species of Sargassum and T.
testudinum were also significant. Specifically, P. sayi chose S. fluitans more than T.
16 testudinum (18 out of 20 or 90%; Z = 3.578; P < 0.001) and S. natans more than T.
testudinum (20 out of 20 or 100%; Z = 4.472; P < 0.001). There was no significant
selection differences between S. fluitans and S. natans by P. sayi, although S. fluitans was
chosen more than S. natans (14 out of 20 or 70%; Z = 1.789; P = 0.07). Comparisons
between male and female crabs showed no significant difference in habitat selection
(Table 5; Fisher’s Exact test, P > 0.05). Crab sizes and weights also had no significant
effect on habitat preferences (Table 5; Logistic regression, P > 0.05 for both).
Control trials showed that P. sayi significantly selected zones with habitats over
empty zones for all four treatments (Figure 8). Specifically, P. sayi chose S. fluitans more
than the control (17 out of 20 or 85%; Z = 3.131; P = 0.002), S. natans more than the
control (19 out of 20 or 95%; Z = 3.859; P < 0.001), artificial Sargassum more than the
control (16 out of 20 or 80%; Z = 2.683; P = 0.007), and T. testudinum more than the
control (18 out of 20 or 90%; Z = 3.578; P < 0.001). There were no significant
differences in choices between male and female crabs or between size and weight of
crabs for the habitat selection control trials (Table 6; Fisher’s Exact test, P > 0.05;
Logistic regression, P > 0.05 for both size and weight).
17 DISCUSSION
Chemoreception experiments
Results of this study show that the Sargassum crab, Portunus sayi, could use
chemical cues alone (i.e., in the absence of visual and direct tactile cues) to distinguish
and select habitats composed of Sargassum spp. These results are consistent with other
studies with decapods. For example, Krimsky and Epifanio (2008) reported that
megalopae of the Florida stone crab, Menippe mercenaria, respond to chemical cues
associated with S. fluitans and that these cues induce megalopae metamorphosis. This
study did not address the specific molecule types involved in this system, but Sargassum
spp. release potentially bioactive molecules such as amino acids and fatty acids,
phlorotannins, and photosynthate (Hanson, 1977; Arnold and Targett, 2000; Wong and
Cheung, 2001; Turner and Rooker, 2006; van Ginneken et al., 2011). Specifically,
Hanson (1977) showed Sargassum releases up to 55% of its photosynthate and Arnold
and Targett (2000) showed Sargassum has high metabolic rates in which 100% turnover
of phlorotannins occurs in 17 days. Although phlorotannins are chemical defense
compounds found in brown algae, there is little evidence that they consistently function
as deterrents in herbivores and have been shown to promote metamorphosis in ascidians
(Tsukamoto et al., 1994). Additionally, some decapods are known to chemically detect
numerous waterborne, organic compounds, including amino acids (Rittschof, 1992;
Markowska et al., 2008). Clearly, the Sargassum crab is detecting molecules exuded from
18 Sargassum. Additional studies should investigate the specific nature of these bioactive
compounds.
The results also showed that although the crab could chemically detect both
species of alga, there was no significant preference for either species based on
chemoreception selection studies. These two species of Sargassum used in this study are
commonly found intermingled in clumps; thus there may be little need for P. sayi to
distinguish between the two species. It is also possible that the chemical composition of
S. fluitans and S. natans are too similar for the Sargassum crab to distinguish differences.
Turner and Rooker (2006) found that the fatty acid composition of S. fluitans and S.
natans are nearly identical.
In trials involving chemical odors from T. testudinum, there was no significant
selection by P. sayi for this seagrass even though T. testudinum contains compounds such
as amino acids and proteins (Burkholder et al., 1959) that decapods are capable of
detecting. As crabs were not attracted or repelled by odors associated with this seagrass,
it is unlikely that P. sayi uses cues from T. testudinum as a potential indicator of an
approaching shoreline. However, this does not rule out the possibility of crabs using T.
testudinum seagrass beds as a habitat when Sargassum is unavailable. Similarly, Krimsky
and Epifanio (2008) demonstrated that stone crab megalopae do not respond to chemical
cues associated with T. testudinum, even though this crab is commonly found in seagrass
habitats.
While the identity and concentrations of chemical odors influencing P. sayi
behavior in this study were not identified, the results clearly demonstrate that molecules
were detected. Other factors that might influence crab behavior include additional
19 chemical cue sources within the Sargassum mats, such as cues from conspecifics and
heterospecifics, and other sensory cues such as visual and tactile cues. Interestingly,
chemical cues in the absence of visual cues were not used by the Sargassum shrimps, L.
tenuicornis and L. fucorum, to locate Sargassum mats (Jobe and Brooks, 2009). Clearly,
habitat location by fauna inhabiting these algal mats involves multiple strategies beyond
chemoreception exclusively. Although molecules are available for detection, crabs may
be unable to locate a chemical source if the direct flow of odors from currents is
unavailable. Future studies on these additional cues and flow patterns would help clarify
the role of chemical-based responses by P. sayi in establishing and maintaining
association with Sargassum mats.
Visual reception experiments
Results from these trials demonstrate that P. sayi can use vision alone (i.e., in the
absence of chemical and direct tactile cues) to locate a habitat, but did not visually
distinguish between S. fluitans, S. natans, and artificial Sargassum. In contrast, Jobe and
Brooks (2009) showed that Sargassum shrimps, L. fucorum and L. tenuicornis, can
visually distinguish between S. fluitans and S. natans, and these selection patterns are due
to morphological differences. Specifically, the more slender L. fucorum is better
concealed within the thinner blades of S. natans, while the larger L. tenuicornis is better
concealed within the thicker blades of S. fluitans. P. sayi may make distinguishing
between these two algal species a lower priority than simply finding a habitat,
particularly if P. sayi can easily be camouflaged within either species of pelagic
Sargassum.
20 In trials involving Sargassum paired with T. testudinum, there were no resulting
significant selection differences. However, S. natans was initially chosen significantly
more than T. testudinum by P. sayi, but later in trials crabs moved numerous times
between the two choices before eventually selecting one. Crabs presented with visual
cues from their normal habitat but in the absence of chemical and tactile cues were likely
confused and therefore decided to continue exploring. Sargassum has a yellow-brown
coloration and more robust structure compared to the flat green blades of T. testudinum.
Therefore, habitat coloration and structure may have played a role in the initial habitat
selections of P. sayi. Color discrimination has been shown in several crab species
including the blue crab, Callinectes sapidus (Bursey, 1984; Baldwin and Johnsen, 2012),
portunid crabs of the genus Carcinus (von Buddenbrock and Friedrich, 1933; Horridge,
1967), and in fiddler crabs of the genus Uca (Hyatt, 1975; Detto, 2007). In particular,
Baldwin and Johnson (2012) demonstrated that blue crab males, C. sapidus, could
distinguish between red and orange colors using both chromatic and achromatic cues, in
which photographs of female crabs with red and orange claws were used. Recognition of
structural visual cues and shapes has also been demonstrated in several crab species
(Vannini, 1987; Diaz et al., 1994; Diaz et al., 1995; Chiussi, 2003).
Habitat selection experiments
P. sayi was given direct access (i.e., chemical, visual, and tactile cues were all
available) to habitat patches in these pairwise choice trials. Specifically, Sargassum spp.
were chosen significantly more than artificial Sargassum and T. testudinum. These results
differ from the visual reception trials where crabs did not distinguish between live and
21 artificial Sargassum and T. testudinum. Again, in the current trials chemical, visual, and
tactile cues were all available, suggesting that the crabs use multiple sensory cues in
habitat location. However, based on the results of the visual selection trials where
distinguishing specific species was rather obscure, chemical cues are likely involved in
precision decision making by the crabs. A similar study involving the use of stimulus
cues used by juvenile blue crabs, C. sapidus, showed that they orientate toward the
direction of the stimulus and that a hierarchy in responses to odors over visual cues exists
(Diaz et al., 2003). In this study, tactile cues were not separated out of the habitat
selection trials and previous studies have shown the importance of tactile cues used by
decapods for homing, predator avoidance, and prey location and therefore may play a
role in habitat selection by P. sayi. (Wehner, 1992; Crowl and Covich, 1994; Dittel et al.,
1996). Habitat architecture (Hacker and Steneck, 1990) might also influence habitat
selection by these crabs as Sargassum spp. have more fronds that could better conceal
them from potential predators compared to the more open spaces between the T.
testudinum blades. However, this influence may be minor based on the results from the
chemical cues experiments in which crabs responded to Sargassum odors but not to T.
testudinum.
The results from the habitat selection trials also showed that there was no
preference by P. sayi between Sargassum species when all cues were available. This
underscores the point made previously that P. sayi may have little need to select one
species of pelagic Sargassum over another as the two species are commonly found
intermingled. Similarly, Jobe and Brooks (2009) found that two species of Sargassum
22 shrimp showed no selection preference for either of the aforementioned Sargassum
species.
During the control trials for the habitat selection experiments, crabs significantly
selected habitats over the control (e.g. no habitat). These results show the importance of
simply finding a habitat. Although crabs did not significantly respond to odors from T.
testudinum in the chemoreception trials, crabs significantly selected T. testudinum
habitats when alternative habitats were unavailable. This shows clearly that P. sayi may
inhabit seagrass beds when Sargassum is unavailable.
Conclusions
Overall, the ability of marine animals in pelagic waters to locate a suitable habitat
represents a significant undertaking and challenge. Presumably, the methods to do so
include a variety of sensory cues. This study examined the sensory modalities used by the
Sargassum crab P. sayi in locating and selecting Sargassum habitats. Based on the results
of this study, the following model is proposed for habitat location and selection for adult
crabs that have been isolated from their Sargassum algal patches.
Given that isolation from patches can occur at anytime, including night, chemical,
waterborne cues that potentially disperse from algae could signal to the crabs (even in
low light conditions) the general presence of an algal mat composed at least partially of
Sargassum spp. While T. testudinum may also be present, data from this experiment show
no significant chemical response by the crabs to this aquatic plant. Chemoreception could
serve as a longer distance means of initiating search behavior for specific patches
compared to visual cues. Once in the visual proximity of a potential patch, the isolated
23 and still highly vulnerable crab will likely move quickly towards a habitat, continuing to
use chemical cues but now supplemented with visual cues. In the absence of a chemical
source, crabs could still potentially locate a habitat using visual cues Once actual contact
has been made with the new habitat patch, all three sensory cue modalities (including
direct tactile information) can be used to confirm its likely preference of a patch
composed of either species (or both) of Sargassum. Although this study was limited to
adult crabs, it would be interesting to investigate habitat location and selection by larval
stages of this crab, and other fauna associated with pelagic Sargassum mats, too.
24 APPENDIXES
Table 1. Chemoreception results from Fisher’s Exact tests (FET) for male and female crabs,
logistic regression (LR Size) for the effects of size on odor selection of Portunus sayi, and
logistic regression (LR Weight) for the effects of weight on odor selection of P. sayi, where P =
probability.
Chemoreception Experiments
S. fluitans vs. control
S. natans vs. control
T. testudinum vs. control
S. fluitans vs. S. natans
Control: left vs. right
FET
P = 1.0
P = 1.0
P = 1.0
P = 0.303
P = 1.0
25 LR (Size)
P = 0.242
P = 0.527
P = 0.624
P = 0.459
P = 0.873
LR (Weight)
P = 0.192
P = 0.368
P = 0.825
P = 0.792
P = 0.458
Table 2. Visual reception results from Binomial Tests (Z) of Portunus sayi for different habitat
pairings with the corresponding probabilities (P). Numbers in parentheses are equal to the number
of crabs out of 20 that chose each habitat.
Visual Reception Experiments
S. fluitans (13) vs. S. natans (7)
S. fluitans (12) vs. artificial Sargassum (8)
S. natans (11) vs. artificial Sargassum (9)
S. fluitans (12) vs. T. testudinum (8)
S. natans (13) vs. T. testudinum (7)
26 Z
Z = 1.342
Z = 0.894
Z = 0.447
Z = 0.894
Z = 1.342
P(Z)
P = 0.180
P = 0.371
P = 0.655
P = 0.371
P = 0.180
Table 3. Visual reception results from Fisher’s Exact tests (FET) for male and female crabs,
logistic regression (LR Size) for the effects of size on visual selection of Portunus sayi, and
logistic regression (LR Weight) for the effects of weight on visual selection of P. sayi, where P =
probability.
Visual Reception Experiments
S. fluitans vs. S. natans
S. fluitans vs. artificial Sargassum
S. natans vs. artificial Sargassum
S. fluitans vs. T. testudinum
S. natans vs. T. testudinum
FET (Sex)
P = 1.0
P = 0.650
P = 1.0
P = 0.650
P = 1.0
27 LR (Size)
P = 0.789
P = 0.730
P = 0.962
P = 0.670
P = 0.475
LR (Weight)
P = 0.675
P = 0.493
P = 0.569
P = 0.997
P = 0.442
Table 4. Visual reception control results from Fisher’s Exact tests (FET) for male and female
crabs, logistic regression (LR Size) for the effects of size on visual reception of Portunus sayi,
and logistic regression (LR Weight) for the effects of weight on visual reception of P. sayi, where
P = probability.
Visual Reception Controls
S. fluitans vs. control
S. natans vs. control
Artificial Sargassum vs. control
T. testudinum vs. control
FET
P = 1.0
P = 0.5820
P = 1.0
P = 0.5820
28 LR (Size)
P = 0.3501
P = 0.8782
P = 0.5563
P = 0.4959
LR (Weight)
P = 0.5063
P = 0.7011
P = 0.4548
P = 0.4326
Table 5. Habitat selection results from Fisher’s Exact tests (FET) for male and female crabs,
logistic regression (LR Size) for the effects of size on habitat selection of Portunus sayi, and
logistic regression (LR Weight) for the effects of weight on habitat selection of P. sayi, where P =
probability.
Habitat Selection Experiments
S. fluitans vs. S. natans
S. fluitans vs. artificial Sargassum
S. natans vs. artificial Sargassum
S. fluitans vs. T. testudinum
S. natans vs. T. testudinum
FET (Sex)
P = 0.629
P = 0.474
P = 0.582
P = 0.474
P = 1.0
29 LR (Size)
P = 0.325
P = 0.585
P = 0.615
P = 0.227
P = 1.0
LR (Weight)
P = 0.213
P = 0.865
P = 0.926
P = 0.189
P = 1.0
Table 6. Habitat selection control results from Fisher’s Exact tests (FET) for male and female
crabs, logistic regression (LR Size) for the effects of size on habitat selection of Portunus sayi,
and logistic regression (LR Weight) for the effects of weight on habitat selection of P. sayi, where
P = probability.
Habitat Selection Controls
S. fluitans vs. control
S. natans vs. control
Artificial Sargassum vs. control
T. testudinum vs. control
FET (Sex)
P = 1.0
P = 1.0
P = 0.582
P = 0.474
30 LR (Size)
P = 0.132
P = 0.251
P = 0.973
P = 0.375
LR (Weight)
P = 0.109
P = 0.215
P = 0.792
P = 0.114
Figure 1. Four tank experimental apparatus used for chemoreception trials. Opaque partitions in
the choice tank create three semi-enclosed compartments. Arrows indicate water flow and “X”
marks the spot where Portunus sayi was placed at the beginning of an experiment.
31 Figure 2. Visual reception diagram showing the visually divided zones. Plastic containers
remained secured above the water level to prevent interference of chemical cues from the
habitats. Portunus sayi was placed in the center of zone 2 at the beginning of each experiment.
32 Figure 3. Habitat selection diagram showing the visually divided zones. Portunus sayi was placed
in zone 2 at the beginning of the experiment.
33 Figure 4. Chemoreception by Portunus sayi for all four treatments (black = Sargassum
fluitans, grey = Sargassum natans, gridded = control, backward hatched = Thalassia testudinum).
A sample size of 20 was used for each treatment. A significant odor selection was shown (★)
for two of the four chemical odor treatments (P = 0.002, P = 0.007, P = .07, P = 0.18,
respectively).
34 Figure 5. Visual reception trials selected by Portunus sayi for all five habitat pairings (black =
Sargassum fluitans, grey = Sargassum natans, forward hatched = artificial Sargassum, backward
hatched = Thalassia testudinum). A sample size of 20 was used for each habitat pairing. There
was no significant visual selection within the five habitat pairings (P > 0.05 for all).
35 Figure 6. Visual reception control trials selected by Portunus sayi for all four pairings (black =
Sargassum fluitans, grey = Sargassum natans, backward hatched = Thalassia testudinum,
forward hatched = artificial Sargassum). A sample size of 20 was used for each treatment. A
significant visual selection was shown (★) for all four visual reception controls (P = 0.025 , P =
0.007, P = 0.007, P = 0.002, respectively).
36 Figure 7. Habitat selection by Portunus sayi for all five habitat pairings (black = Sargassum
fluitans, grey = Sargassum natans, forward hatched = artificial Sargassum, backward hatched =
Thalassia testudinum). A sample size of 20 was used for each habitat pairing. A significant
habitat selection was shown (★) for four of the five habitat pairings (P = 0.07, P < 0.001, P =
0.007, P < 0.001, P < 0.001, respectively). For the treatment pairing of S. natans and T.
testudinum (on far right), P. sayi chose S. natans for each of the 20 trials.
37 Figure 8. Habitat selection control trials selected by Portunus sayi for all four habitat pairings
(black = Sargassum fluitans, grey = Sargassum natans, forward hatched = artificial Sargassum,
backward hatched = Thalassia testudinum). A sample size of 20 was used for each habitat. A
significant habitat selection was shown (★) for all four habitat controls (P = 0.002, P < 0.001,
P = 0.007, P < 0.001, respectively).
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