Download The following seven species were found on Diopatra

Tool Use by a Predatory Worm
Brian Taylor
Under the supervision of Dr. Rittschof,
Nicholas School of the Environment, Duke University
May, 2016
_______________________________
Research Supervisor
_______________________________
Faculty Reader
_______________________________
Director of Undergraduate Studies
Honors thesis submitted in partial fulfillment of the requirements for graduation with
Distinction in Biology in Trinity College of Duke University
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Abstract
Tool use in non-human organisms represents one of the most fiercely contested topics in animal
behavior research. Tool use by an animal has been claimed to represent an evolutionarily
significant jump in rational thought and ability. Here, I test the hypothesis that Diopatra cuprea
are stay-at-home predators who use algae, shells, and sticks as a tool to decorate their tubes in
order to serve as an advertisement for attracting prey. Diopatra are a sedentary, tube-dwelling
annelid found in great abundance along the intertidal zone. These worms construct and live in
long tubes, with the majority of the tube below the sediment surface and a small portion
exposed above ground. They then decorate the exposed portion with three different
materials: algae, shells, and sticks. To test this hypothesis, I determined what microorganisms
took up residence on Diopatra tubes, analyzed the rate at which the worms rebuilt their tubes,
and observed the feeding behavior of Diopatra. I found that the same group of microorganisms
lived on all three decoration types, but in differing quantities. I also found that if a worm had the
exposed portion of its tube destroyed by a disturbance event, it would rebuild the tube almost
immediately. I was able to observe Diopatra eating off of their tubes in the laboratory setting and
then experimentally determine what their likely food sources are, leading me to the conclusion
that the decoration on their tubes serves as a tool for the worms and plays a vital role in their
feeding behavior.
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Introduction
Diopatra cuprea is an easily overlooked organism, small in size and largely ignored in
discussions of the coastal ecosystem. As a result, comparatively little is known about them.
Known often as the decorator worm, it is a tube-building worm found in the intertidal zone along
the eastern coast of the United States, from Massachusetts to Brazil (Berke, 2012). About 5 cm
long at maturity, Diopatra live in a self-engineered tube that it decorates with debris from the
sediment surface (Myers, 1972; Berke, 2012).
Much of the research on Diopatra has focused on the unique nature of their tubes and the
role they play in providing both a habitat and defense from predation for the organism
(Brenchley, 1976; Berke & Woodin, 2008). Given the enormous amount of energy that the worm
invests not only in constructing its tube but also in decorating the tube, I suspected that the tube
must serve an additional function for the worm. Previous researchers had offered a number of
hypotheses for why Diopatra decorate the outside of their tube, ranging from attracting prey
(Myers, 1972) to providing additional defense (Brenchley, 1976; Endler, 1981) to serving as
camouflage to disguise the tube (Klingel, 1951). Dr. Daniel Rittschof and I hypothesized that the
decoration of the exterior made the tube a tool for the worm, allowing it to imitate a micro reef
and attract microorganisms to live on it.
A reef is defined as a rock collection containing the remains of colonial organisms that
attracts diverse organisms and fauna to live on it (Wilson 1950). The exterior of a Diopatra’s
tube resembles a micro reef in that the worm attaches algae, shells, or sticks to it, which we
hypothesize is an attempt to attract other organisms to live on the tube. As Reisser et al
demonstrated in their 2014 paper, small millimeter-sized objects floating in the ocean attracted a
variety of microorganisms to successfully live on their surface. This indicates that it is feasible
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for a Diopatra worm to assemble a collection of small objects and use them to decorate the
exterior of its tube with the intention of cultivating a collection of microorganisms.
In this discussion, decorating refers to an action in which the worm extends out of its
tube, picks up or pushes a piece of shell, rock, sand, or other object to the tube, and adheres it to
the tube with a glue the worm secretes from glands in its body (Myers, 1972). Diopatra tubes
have decorated and undecorated sections. The decorated region is the part of the tube above the
sediment surface (Myers, 1972). The undecorated section comprises the majority of the tube and
is mainly found below the sediment surface (Myers, 1972). This portion serves as a home during
low tide and a shelter from predators when the tide is higher (Myers, 1972; Brenchley, 1976;
Berke & Woodin, 2008). These sessile, predatory worms are mostly active in the decorated
portion of their tube during high tide when they extend themselves out into the water column.
They then retreat back into the undecorated tubes as the water recedes and the decorated region
is exposed to air (Klingel, 1951).
Diopatra select a decorating material for its tube based on the abundance of surrounding
material (Brenchley, 1976). The worms do not appear to show any predisposition to a particular
decoration type or decorate selectively, other than with respect to the size and proximity of
available resources (Berke, 2012). For Diopatra, there are three main natural categories of
decoration materials, which are referred to as stick, shell, and algae. The stick group is
comprised of small fibers such as roots, the shell group is made up of any small shells commonly
found on the ocean floor, and the algae mainly consist of pieces of macroalgae. Depending on
the habitat, the frequencies of these decorating materials vary. In addition, any small structure
like a piece of ribbon or plastic discarded on the beach can also be used for decoration by the
worm.
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Tool Use by an Organism
Tool use in non-human organisms represents one of the most fiercely contested topics in
animal behavior research (Shumaker, 2011). Tool use by an animal has been claimed to represent
an evolutionarily significant jump in rational thought (Andrews, 2014), and while it was
previously claimed that only humans possessed the skill to use tools (Beck, 1980), more recent
ideas have allowed the possibility that some other animals are also capable of using tools
(Bentley-Condit & Smith, 2010). One of the underlying questions in determining if an animal is
in fact a tool-using organism is whether it is manipulating an object to act as a tool or simply
using the object as a resource (Goodall, 1970). In other words, is the object in question a
replacement for a natural behavior in order to make a task more achievable? For example, the
Galapagos woodpecker finch is considered a tool-using organism because it holds a cactus spine
or twig in its beak and uses it to poke inside holes of tree bark and force insects out for the bird
to eat (Bock, 1963). On the other hand, a bird using sticks to create a nest is not considered toolusing because the sticks are merely being used for assistance; the claws and beak of the bird are
the actual tools that make the nest and the sticks are merely a resource.
I put forth the hypothesis that Diopatra are not just using the shells, sticks, or algae as
objects to assist their tubes but rather are manipulating them to function as a tool. These objects
are repurposed by the worm to imitate the appearance of a naturally occurring micro reef in order
to attract prey to live on them. As a result, they improve the fitness of the worm by allowing it to
become a stay-at-home predator.
Examining Tool Use in Diopatra Cuprea
We were curious about the lifestyle of Diopatra and how a largely sessile predatory
worm was able to obtain its prey without leaving the safety of its tube. We decided to test the
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hypothesis that Diopatra is a tool-using organism. Specifically, I tested the hypothesis that the
decorated exterior portion of their tube is a tool used by the worm to imitate a micro-reef from
which they harvest prey.
In order to test this, I first examined tubes in the lab in order to identify potential fitness
differences between the three materials the Diopatra used to decorate the exterior of their tubes. I
also measured the length of the tubes to determine if the size of the exposed portion played a role
in the number of organisms present. Additionally, I determined the presence of microorganisms
on the exterior of the tube that could serve as potential sources of prey. Then, I studied tube
rebuilding through tube removal experiments in the field in order to determine the rate and
relative importance of reconstructing a damaged tube. Finally, in laboratory experiments I
observed and quantified predation of the four most common occupants of the micro-reefs by the
worm.
Methods
Tube Collection
Diopatra tubes were collected from intertidal regions around Pivers Island, North
Carolina at low tide. Only the portion of the tube above the sediment surface was collected. Each
tube portion was cut off at the sediment surface and placed into its own 50 mL centrifuge tube to
prevent cross contamination. Tubes were stored in the lab at room temperature. The length of
each tube portion was measured and recorded. Ten tubes of each decoration type (algae, shell,
and stick) were collected in two groups of thirty, for a total of sixty samples. Additional tubes
were collected separately using the same technique in order to gather prey as explained in the
“Prey Introduction” section.
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Decoration Type
The type of worm tube – algae, shell, or stick – was determined through taking
photographs of the decoration of thirty tube caps. The surface area of each decoration type was
measured utilizing ImageJ. Tubes were first classified by primary decoration type in order to
provide a baseline category for future experiments. The makeup of a generic tube was then
determined by calculating the average quantity of each decoration type in three different
environments: high energy, medium energy, and low energy. The energy of an environment was
determined based on the surrounding water flow.
Tube Rebuilding
Thirty exposed portions of tubes (ten of each decoration type) were measured and cut at
the sediment surface during low tide. Tube locations were marked and the length of the new
decorated section of the tube above the sediment surface was measured at each subsequent low
tide until the tube had returned to a length similar to the original. This measurement aided in
calculating the rate of reconstruction. The decoration materials of the new tubes were identified
and compared to the original cut tubes.
Prey Identification
The tubes were individually treated with 95% Ethanol, filtered through a four by four
micron sieve, and stained with rose-bengal to facilitate the identification of organisms living on
the tube. Stained invertebrates were counted and imaged under a microscope at 52x
magnification.
Prey Introduction
The prey identification experiments yielded four potential food sources for the worm:
copepods, nematodes, gastropod larvae, and amphipods. Large quantities of each species were
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collected from Diopatra tubes to test if Diopatra would eat them. The prey was collected from
the exterior of tubes using the same method described in the previous sections. The obtained
solutions were then examined under a microscope at 52x magnification and a micropipette was
used to extract the tagged organisms from the solutions and separate them by species.
Ten live Diopatra were collected in their tubes by using a shovel at low tide to dig up
about 16 cm of undecorated tube containing the worm. Worms, in their individual tubes, were
placed in 10 cm diameter finger bowls filled with seawater and left undisturbed for 24 hours
before testing.
Stained prey candidates were then introduced onto the tubes. Ten of each candidate was a
large enough quantity as to be in excess of what would be found in nature. This was done to
provide the worm with ample food in order to facilitate observations of Diopatra eating
behavior. The stained prey was left on the tubes for a period of 24 hours, after which the tubes
were collected and rinsed with EtOH. The tubes were then examined under a microscope at 52x
magnification to determine what the worms had eaten and what they had left behind on the tube.
The number of stained organisms that remained were then counted and compared to the amount
originally added.
Results
Decoration Type
Diopatra tubes were divided into three categories based on the area that they were
gathered: high energy, medium energy, and low energy. As shown in Figure 1, the average high
energy Diopatra tube was decorated with 52.9% shell, 22.2% stick, and 24.8% algae; the
average medium energy tube was decorated with 58.7% shell, 24.6% stick, and 16.7% algae; the
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average low energy tube was decorated with 47.1% shell, 35.7% stick, and 17.1% algae. Overall,
the average tube was decorated primarily with shells and most sparingly with algae.
Figure 1. Decoration of Average Tube
High Energy Tube Decoration
70
% of Tube
60
50
40
30
20
10
0
Shell
Stick
Algae
Decoration Type
Medium Energy Tube Decoration
80
% of Tube
70
60
50
40
30
20
10
0
Shell
Stick
Decoration Type
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Algae
Low Energy Tube Decoration
60
% of Tube
50
40
30
20
10
0
Shell
Stick
Algae
Decoration Type
Figure 1. Shows the average surface area of tube tops covered by shell fragments, dead fibrous
vegetation, and living algae.
Table 1. Comparison of Average Tube Length and Average Number of Organisms
Decoration Material Length (mm) Number of Organisms
Algae
29.8
13.2
Stick
30.3
8.4
Shells
30.6
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Table 1. Examines the relationship between tube length and average number of organisms
between the three decoration types
As shown in Table 1, tubes decorated with algae were found on average to contain the
greatest amount of microorganisms, while tubes decorated with shells contained the least.
However, as shown in Figure 1, algae was not the most commonly utilized decoration material.
Despite this apparent advantage, no evidence was found to indicate that algae or any particular
decoration material is preferred by the worm. This would suggest that there is no discernable
fitness difference between the three materials and that decoration type appears to be determined
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only by the quantity and nature of available resources, rather than by a worm’s decision to favor
one material over another
Tube Length
Table 1 shows the average length of the decorated portion of Diopatra tubes in
millimeters and the average number of organisms found on the tube. Stick-dominated tubes had
the greatest length while shell-dominated tubes were the shortest in length. Tubes composed
mainly of algae had the largest number of organisms followed by sticks. Shell decorated tubes
had the least number of animals.
Tube length does not appear to be a large factor in determining the number of organisms
present on the exterior of a Diopatra’s tube, as there was no clear relationship between increased
tube length and quantity of organisms. The number of organisms present appears to be related to
the type of decoration material; tubes decorated with algae were the shortest on average but had
the greatest number of organisms, while tubes decorated with shells were on average the longest
but had the fewest organisms. Additionally, there is no evidence that Diopatra vary the length of
their tubes in response to the relative success of their decoration material.
Tube Rebuilding
The following figures show the average length of the tubes above the sediment surface at
each subsequent low tide as grouped by predominant decoration type. Of the original thirty tubes
that were collected, twenty were rebuilt with the same type of decoration material, four were
rebuilt with different types of decoration material, and six were not rebuilt at all. All tubes were
reconstructed to a relatively similar size as the original.
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Figure 2. Average Rate of Tube Rebuilding Separated by Decoration Type
Average Rate of Tube Rebuiliding
40
Tube Length (mm)
35
30
25
Algae
20
Sticks
15
Shells
10
5
0
Original
0
1
2
3
4
5
Low Tides Since Tube Cut
Figure 2. Shows the length of Diopatra tubes measured from the sediment surface to the end of
the tube. Tubes were measured to obtain an original value and then cut and measured at each
subsequent low tide to track average rebuilding rate. Each bar represents the average length of
ten tubes of the same decoration type. Results are separated by the primary decoration type of the
original tube.
Prey Identification
The following seven species were found on Diopatra tubes: copepods, nematodes,
gastropod larvae, amphipods, polychaetes, barnacle larvae, and Geukensia. Organisms found on
tubes were identified based upon physical appearance under a microscope at 52x magnification.
Of the seven identified species, four of them always appeared to be present regardless of
decoration type, water energy, or tube length: copepods, nematodes, gastropod larvae, and
amphipods. These four organisms were hypothesized as potential prey sources and collected for
further examination.
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Figure 3. Organismal Diversity on Diopatra Tube
Number of Organisms/Tube
Organismal Diversity on Diopatra Tube
7
6
5
Algae
4
Stick
3
Shell
2
1
0
Species
Figure 3. Shows the average number of organisms by species on Diopatra tubes, differentiated
by decoration type. A tube was classified as primarily decorated by a particular decoration type if
upon visual inspection that decoration was clearly dominant. Copepods, nematodes, gastropod
larvae, and amphipods were present on nearly all sampled tubes.
Food Introduction Tubes
Stained prey of the four candidate species were collected and introduced onto the exterior
of Diopatra tubes in the lab setting in order to observe which organisms were consumed by the
worm. Figure 4 shows the remaining stained prey that were found on the Diopatra inhabited
tubes after a period of 24 hours. The species were identified through examination under 52x
magnification. Copepods and nematodes were found to be consistently consumed by the worm,
while gastropod larvae and amphipods were present in roughly their original quantities. The
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slight decrease in the presence of gastropod larvae is hypothesized to be experimental error in
sample collection rather than a significant result.
Figure 4. Number of Species Remaining After Predation
Number of Organisms
Comparison of Potential Food Sources
10
9
8
7
6
5
4
3
2
1
0
Starting
Quantity
Remaining
Quantity
Copepod
Nematode
Gastropod
Larva
Amphipod
Candidate Prey Species
Figure 4 Shows the average number of each of the four candidate prey species remaining
twenty-four hours after being introduced onto the exterior of a Diopatra tube in the lab setting as
compared to the original introduced quantity.
Discussion
Tube Decoration
Diopatra tubes are more than just a home, they are a tool for the worm to collect prey.
Diopatra decorate their tubes primarily with three distinct materials: shells, sticks, and algae.
While tube length was relatively similar across all three decoration types, the number of
organisms found residing on the outside of the tube was different. Tubes decorated with shells,
which were the most commonly found tubes on the beach, had significantly fewer organisms
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present (average of 6 organisms per tube) than those decorated with algae (average of 13.2
organisms per tube), which were the least commonly found. Therefore, it appears that the
relative abundance of shell decoration is due primarily to the availability of decoration material
in the surrounding environment (Brenchley, 1976), as shells do not appear to convey any fitness
advantage to the Diopatra, despite being the most commonly found decoration type on the beach
where the samples were gathered.
The different types of tube decoration influence the quantity of microorganisms present
on the exterior of the tube, however they do not appear to convey a direct fitness advantage. This
shows that the worm has little to no ability to select for its decoration type because although
algae was the most successful decoration, it was also the least common, while the least
successful decoration of shells was the most common. This may also suggest that the increased
number of organisms on the tubes decorated with algae does not benefit the Diopatra in any
way, and that the number of organisms present on the tubes decorated with shells is sufficient
food for the worm. Furthermore, the consistency of tube height across all decoration types
indicates that increasing the size of the tube is not a viable strategy for the worm to increase the
success of a tube decorated with shells or sticks, implying that there is likely some upper bound
or optimal size for the exposed portion of the tube.
Previously, most researchers had hypothesized that tube decoration was for camouflage
(Endler, 1981, Stowe, 1988, Berke & Woodin, 2008, Brenchley, 1976). Brenchley hypothesized
that the worm decorated with materials according to relative abundance in order to blend in with
the natural environment (Brenchley, 1976). Berke & Woodin tested the hypothesis that
decoration provided camouflage and found that undecorated tubes were not attacked more
frequently than decorated tubes (Berke & Woodin, 2008). Furthermore, undecorated tubes were
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actually at less risk of attack than tubes classified as predominantly algae or shell (Berke &
Woodin, 2008). All of these findings would seem to indicate that Diopatra do not decorate their
tubes as a means of camouflage, as at best it has no effect on predation and at worst it places
them at greater risk of attack.
Tube Regeneration
If the Diopatra’s tube does in fact serve as both a habitat and prey catcher for the worm,
its existence is critical to the worm’s survival. As a result, it is expected that if the exposed
portion of the tube were to be removed, the worm would immediately replace it. Failure to do so
would likely result in starvation. To test this theory, I measured and marked thirty different
Diopatra tubes (ten of each decoration type) and then removed the exposed portion of the tube at
low tide in order to simulate a naturally occurring disturbance event. The tubes were then
observed at each subsequent low tide to track their reconstruction process.
It was found that twenty-four of the thirty tested tubes were already in the process of
being reconstructed and six had no activity, likely indicating that there was no worm present. On
average the worm was able to rebuild approximately 6-8 mm worth of exposed decorated portion
of their tube in one low tide cycle. This rate of reconstruction remained relatively consistent over
the next four low tides and by the fifth low tide all the inhabited tubes had returned to a
functional level that was relatively similar to their initial length with no measurable length
difference on the sixth low tide. Additionally, it was found that twenty of the newly exposed
portions were decorated with the same material as the original exposed segment, while only four
tubes had changed decoration material. This further supports the theory that tube decoration is
determined by the proximity of resources rather than any preferences of the Diopatra.
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Prey Identification
An analysis of the organisms found on the outside of the tubes revealed that seven
organisms were most commonly found: copepods, nematodes, gastropod larvae, amphipods,
polychaetes, barnacle larvae, and Geukensia. Due to the relative frequency of copepods,
nematodes, gastropod larvae, and amphipods as well as their consistent appearance across tubes
and decoration types, they appear to be the most likely candidates for the Diopatra food source.
As a result, these four species were further examined and used in the feeding trials to determine
what Diopatra consume.
By exposing Diopatra to a high concentration of their four most likely food sources, I
hoped to observe and calculate what the worms eat. Ten individuals of each of the four candidate
prey species were introduced onto the exterior of Diopatra tubes in the lab setting. The prey
species were left on the tubes for twenty-four hours to allow ample time for normal feeding
behavior. At the end of the twenty-four hour period the tubes were rinsed with ethanol to collect
everything on the exterior of the tube.
Upon analyzing the data, it was found that both copepods and nematodes were consumed
at significantly higher rates than gastropod larvae and amphipods. On average, the worm ate 69%
of the introduced copepods and 59% of the available nematodes, while nearly all of the
gastropod larvae and amphipods were left behind. This would indicate that both copepods and
nematodes serve as the primary food sources for the Diopatra, as they were both shown to be
eaten by the worm and found in abundance on all three decoration types.
Tubes as Farms
It has been experimentally shown that a greater number of species accumulate near
clumps of Diopatra tubes than elsewhere (Woodin, 1981). However, this seems counterintuitive
15
if the Diopatra feeds off these microorganisms. Two hypotheses have been proposed to explain
this anomaly: the refuge hypothesis and the larval accumulation hypothesis, both of which may
be true (Woodin, 1981).
The refuge hypothesis draws largely on foraging theory, which puts forward the idea that
the likelihood of an organism being preyed upon is related to the amount of time and energy a
predator must expend in order to capture that particular organism relative to another (Woodin,
1981). Ultimately, to avoid predation an organism does not need to be able to avoid the predator,
but rather to outrun other potential prey. Diopatra tubes provide greater habitat complexity than
a sand water flat habitat, thus increasing epifauna predatory time and the energy level needed to
reach prey (Woodin, 1981). Brenchley also spoke of this habitat complexity, explaining that
Diopatra created a heterogeneous, complex “structural refuge” that differs from the
homogeneous, local habitat (Brenchley, 1976).
The larval accumulation hypothesis revolves around flow dynamics, stating that
microfauna are not drawn to the decoration of the exterior of the tube, but rather end up on the
tube by chance (Woodin 1981). The worm’s tubes disrupt the normal flow of water as it sticks
out above the sediment surface, causing a higher number of species larvae to passively
accumulate on the tubes (Woodin, 1981).
I propose a modification to the refuge hypothesis presented by Woodin, which is that
Diopatra are tool-using organisms that decorate their tubes in such a way as to appear to offer a
refuge to microorganisms, but ultimately to act as farms in order to attract epifauna to live on
them. The presence of a Diopatra tube creates a relative abundance of epifauna on and around
the tube due to the protection the tube offers from predation (Woodin, 1981). This security
comes at a cost, however, as the epifauna trade predation from other organisms for predation
16
from the Diopatra. It is therefore hypothesized that the relative rate of predation on epifauna by
the Diopatra is less than the normal rate of epifaunal predation in a standard sand flat
environment. Ultimately, the epifauna benefit from living on the tube rather than in the sand, and
the Diopatra benefit by having a steady source of food available to them.
Tool Use
An organism can be considered a tool-using organism if it is manipulating an object to
replace a natural behavior in order to make a task more achievable. A Diopatra is a tool-using
organism because it utilizes the shells, sticks, and algae as a tool in the same way as the
Galapagos woodpecker finch. Just as the finch holds a cactus spine or twig in its beak and uses it
to poke inside holes of tree bark and force insects out for the bird to eat, the worm is
manipulating the shells, sticks, and algae to decorate the exterior of its tube and attract prey. In
both organisms, the utilization of the object replaces natural hunting behavior in order to make
the task of acquiring prey more easily achievable. Without the decoration, the microorganisms
would not take up residence on the exterior of the tube, just as without the twig the finch would
not be able to force its prey out of hiding. Diopatra cuprea use the decoration as a tool in order
to attract prey and improve their own success as a species. As a result, Diopatra can be
considered a tool-using organism that builds a micro-reef in order to attract its prey to live within
reach.
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