Predator interactions among green crabs (Carcinus maenas) and dogwhelks (Buccinum undatum) in the presence of blue mussel (Mytilus edulis) prey

Rachel BrodieSeptember 22, 2012

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Abstract

In many coastal marine environments, blue mussels (Mytilus edulis) play a critical role in

determining the biodiversity and providing a basal food source for many predators. The

present study examined the effects on mussel predation by single and multiple predator

systems of green crabs (Carcinus maenas) and dogwhelks (Nucella lapillus). Total number and

mean size of mussels consumed by each species was determined for comparison between

single and multiple predator treatments. Feeding rates of whelks decreased significantly in the

presence of green crabs. The presence of whelks had a positive effect on crab foraging, in

which higher mussel consumption was approaching significance for crabs experiencing

interspecific competition for food in comparison to crabs only competing with conspecifics.

There was no statistically significant difference between the sizes of mussels consumed in each

treatment. When comparing the mean number of mussels consumed for each treatment,

significantly more mussels were consumed in multiple-predator treatments. Results indicate

that the presence of another predator has a significant impact on the feeding pattern of other

invertebrate predators of blue mussels. Interspecific predator interactions are therefore an

important part of mussel bed community dynamics.

1. Introduction

Community dynamics are impacted by predation, competition, species diversity and

species density (McQueen et al., 1989). In natural systems, most prey face risk of mortality

from a variety of different predators. Predators may interact while foraging, causing a

deviation from the predicted consumption when the activity of isolated predators is summed

(Sih et al., 1998). When risk reduction is observed, the number of prey consumed is less than

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predicted from isolated predators due to the interactions between predators or prey behaviour

reducing foraging rates (Griffen and Byers, 2006). On the contrary, risk enhancement results

when prey behaviours or competitive predator facilitation increases foraging success (Mansour

and Lipcius, 1991). Predator facilitation is an example of a positive interaction within

community dynamics, in which the presence of one species assists the ability of another species

to forage (Soluk, 1993). Non-independent multiple predator effects on prey can include both

conspecific and interspecific pairs of predators (Wong et al., 2010). When the observed and

predicted consumption rate differs for conspecific and interspecific predator cases, the effects

of multiple predator species is evident (Vance-Chalcraft et al, 2004). This indicates that the

effects of interspecific predators on consumption rates are independent of predator density.

Filter-feeding invertebrates serve as the key basal food source for a variety of different

food web interactions within intertidal communities (Menge and Branch, 2001). Intertidal

communities are often used to investigate the effects of predation, competition, and various

other interactions among predators and prey. This environment provides many benefits to

ecologists, including small, sessile or slow moving organisms which can be easily manipulated, a

simple assemblage, and predators that often share a similar resource which commonly causes

high levels of competition (Bertness et al., 2002). The blue mussel Mytilus edulis is present in

dense beds in the intertidal zone and helps to support rich communities of species in

Passamaquoddy Bay, Bay of Fundy, Canada (Quinn et al., 2012). Blue mussels are abundant

filter feeders in this region and are predated upon by dogwhelks (Buccinum undatum), sea stars

(Asterias spp.), and green crabs (Carcinus maenas) (Hamilton, 2000).

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The green crab is an invasive decapods crustacean that originated from Europe and

Northern Africa (Jensen, et al 2007). Crabs are highly aggressive competitors, with interference

by conspecifics potentially inhibiting crab feeding (Griffen and Williamson, 2008). The green

crab is an omnivorous predator feeding primarily on bivalves, but also on plants, small

arthropods and gastropods (Ropes, 1968).

Dogwhelks are carnivorous gastropod molluscs that feed on mussels, periwinkles, and

barnacles (Crothers, 1985). In order to search and consume prey, whelks utilize both physical

and chemical techniques. Olfactory chemical senses lead whelks to food sources, where they

use a combination of chemical dissolution and radular scraping to bore through the shells of

prey (Carriker and Williams, 1984). Foraging by whelks has been found to be impacted by intra-

and interspecific interactions. Dogwhelks are occasionally eaten by green crabs; this is an

example of intraguild predation (Trussel, et al., 2003). Chemical risk cues in the seawater serve

as a signal to dogwhelks that predatory crabs are present in their environment. Dogwhelks

often respond to these risk cues by reducing their feeding rate. The presence of other

dogwhelks can also impact foraging activity. Chemical cues from feeding whelks have been

suggested to stimulate conspecifics to feed (Dunkin & Hughes, 1984). The same principle may

be at play for crabs as they use olfaction to detect prey (Crothers, 1985).

Along the mid-Atlantic coast of North America, two of the most common predators of

mussels are the green crab and the dogwhelk (Crothers, 1968). Two studies have been

conducted on the competition between green crabs and dogwhelks in an intertidal community

near St. Andrews, New Brunswick. d’Entremont (2005) performed a field and lab experiment to

investigate the effect of competition and density of predators on the level of consumption of

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blue mussel prey. d’Entremont found that whelk feeding was depressed by crab presence, but

crabs were unaffected by the presence or absence of whelks. A field study conducted by Quinn

(2012) looked at the interactions between two blue mussel predators, the green crab and

dogwhelks. In contrast to the findings in 2005 by d’Entremont, Quinn found that crabs in the

presence of whelks tended to consume more biomass than in the whelk-free treatments.

The aim of this project is to examine the interspecific interactions on feeding rates. It is

hypothesized that negative interactions between predators at high densities will lead to

depression of foraging rates in comparison to single-predator treatments. It is predicted that

interspecific competition will cause a decrease in whelk feeding rates because of the presence

of crabs and associated crab risk cues. Competitive intra- and interspecific interactions at high

densities is also hypothesized to cause predators to alter prey size selection in order to

minimize competitive interactions. It is predicted that predators will become less selective

under higher competitive stress of interspecific competition and feed on mussels of sub-optimal

sizes.

The conflicting results of these green crab-dogwhelk interactions have inspired a further

investigation into the effect of competition on their feeding rates. Understanding what affects

predation rates helps us gain a better understanding of entire systems. It is important to

recognize that predators not only have an obvious effect on their prey, but also on each other.

These predation rates dictate the density of the mussel bed, and therefore the structure of the

entire mussel bed community.

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2. Materials and Methods

2.1 Experimental Setup

Experiments were conducted at the Huntsman Marine Science Center, St. Andrews,

New Brunswick, Canada. Green crabs, dogwhelks and mussels were kept in separate 30cm x 60

cm aquaria in a flow-through set up for five days prior to experimental trials. Predators were

starved for this five day period to standardize hunger levels and to acclimate them to lab

conditions. During experimental trials, species were placed in a flow-through aquarium

measuring 30cm x 60cm. In the center of the each aquarium was a 10cm x 30cm tile where

mussels attached. This arrangement allowed for foraging to take place within an area of

0.03m2, consistently across all tanks. Black covers were placed over each tank during

experimental trials to exclude external variables, such as movement, view of other predators in

adjacent tanks and changes in light exposure. Water temperature of all trials and holding tanks

remained fairly consistent ranging from 14-14.5⁰C.

2.2 Treatments

Predator densities were determined based on the area of the tile (0.03m2), in which all

foraging predator interactions would take place. The density of all predator species was kept at

a consistent level in order to specifically examine the effect of the presence or absence of

another predator on feeding rates. High predator density was based on analysis of the littoral

zone of Passamaquoddy Bay in the Bay of Fundy conducted by Quinn (2012). To achieve a high

density of predators based on Quinn (2012), the number of predators used within the 0.03m2

foraging area was 2 green crabs and 7 whelks. Mussels per aquaria should be approximately 50

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individuals to reflect normal distribution in natural environments (Boudreau, 2011). However,

due to resource limitations, only 36 mussels were added to each tank.

Mussel-covered tiles and predators were randomly assigned to one of three

treatments. Experimentation was conducted from August 13-16, 2012. Eight replicates were

completed for each treatment. There were three different treatments examined: 1) only

dogwhelks observed at a high density (7) with blue mussels, 2) dogwhelks (7) and green crabs

(2) together at a high density with blue mussels, and 3) only green crabs at a high density (2)

with blue mussel prey. Treatments with single predator species (1 and 3) tested the effects of

intraspecific interactions on predator foraging, while treatment 2 with both predators present

tested the effects of interspecific interactions on mussel consumption.

2.3 Predator and Prey collection

All species were collected within the intertidal zone at Indian Point in St. Andrews, New

Brunswick, Canada. Collections took place at low tide from August 7-10, 2012. Crab sizes were

within a range of 48-68mm in carapace width. To avoid any behavioural or morphological

biases, only male crabs were used. Dogwhelks ranged from 25-40mm in height. Mussels were

collected and ranged in size from 30-50mm. These specific ranges in species size ensure that

prey species are edible by both predator species (Quinn, 2010).

2.4 Data Collection

The duration of each trial was 12 hours. After each test, all predators and mussels were

removed for analysis. Mussels with at least one bore hole in an otherwise intact shell were

classified as killed by a whelk. A mussel shell with chips was classified as being consumed by a

crab. This sorting method is consistent with the method outlined by Quinn (2012).

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The total number of mussels consumed by each species in single and multiple-predator

treatments was recorded. The size of mussels that were consumed was also measured.

2.5 Statistical methods

All statistical analysis was carried out using SPSS 20 IBM processor. A univariate ANOVA

test was used to compare the mean number of mussels consumed in the presence of only

whelk predators, only green crab predators, and when both whelk and green crab predators

were present in foraging areas. The mean number of mussels consumed was normally

distributed according to the Shapiro-Wilk test of normality (p-value: 0.091). Post-Hoc

comparisons between the three treatments were performed using Tukey’s HSD test. A 2-factor

ANOVA could not be used to test the interaction between crabs and whelks due to limited

degrees of freedom.

The mean number of mussels consumed by whelks in each treatment was not normally

distributed according to the Shapiro-Wilk test of normality (treatment 1 p-value: 0.04,

treatment 2 p-value: 0.00). Thus, a non-parametric Kruskal-Wallis test was performed to

examine the impact on dogwhelk foraging rate in single and multiple-predator treatments.

To examine the relationship between crab consumption and predator environment, a t-

test was performed to compare the mean number of mussels consumed by crabs when

dogwhelks were present (treatment 2) in comparison to crab-only predators (treatment 3). A

parametric t-test was used because mussels consumed by crabs in treatment 2 and 3 passed

the Shapiro-Wilk test of normality (treatment 2 p-value: 0.792, treatment 3 p-value: 0.162).

Comparison between the sizes of mussels consumed by each predator in all treatments

was examined using a univariate ANOVA test, since the data was normally distributed according

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to the Shapiro-Wilk test of normality (treatment 1 p = 0.740, treatment 2 p = 0.954, treatment 3

p = 0.380). A t-test was used to specifically analyze the prey size selection of crabs between

treatment 2 and 3.

3. Results

Four main questions were examined in this study. The first question examined the

effect on prey risk when treatments included only conspecific predators in comparison to when

predators experienced interspecific interactions. The difference between overall consumption

of mussels when both predators are present, in comparison to single predator treatments is

shown in figure A1. It is observed that when dogwhelks and green crabs are both present, prey

risk is enhanced and therefore the number of mussels consumed is significantly greater than

when only one predator species is present (Figure A1a). A Post-Hoc Tukey HSD test was

performed, in which the mean number of mussels consumed for the interspecific predator pair

(treatment 2) was significantly higher than the conspecific predator treatments (1 and 3)

(Tukey’s HSD test, p=0.003, Figure A1a). When each species is examined separately, crab

foraging rates appear to be higher than foraging rates of whelks. When both predators are

present in treatment 2, crab consumption of mussels is greater than the amount of mussels consumed

by whelks (Figure A1b).

The second question asked in this study focuses on the feeding rate of dogwhelks. The

impact on foraging rate of dogwhelks was examined when only conspecifics were present in

comparison to the consumption of dogwhelks when green crabs were also present in the

foraging area. Figure A2 depicts the significant difference found by the Kruskal-Wallis test,

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where feeding rates were significantly lower for whelks which had crabs present (x2 = 9.734, df =

1, p-value = 0.002).

The third question asked by this study was specific to green crab feeding rates. Figure

A3 shows the comparison between the mean number of mussels consumed by crabs

experiencing intra-and interspecific competition (treatment 2) in comparison to consumption

by crabs only competing for food resources with conspecifics (treatment 3). As observed in

figure A3, the mean number of mussels consumed by crabs in the presence of whelks was

higher than crabs without whelks present, and this difference is approaching significance (t =

2.093, df = 13.217, p-value = 0.056).

The final question that was explored in the present study was the matter of mussel size

consumed by each species in different predator systems. Figure A4 depicts the mean size of

mussels consumed for each treatment. The mean size of mussels consumed by whelks in

treatment 1 is higher than all other treatments, but this is not statistically significant (F= 1.664,

p-value = 0.215). Therefore, predator treatment did not significantly affect the mean size of

mussels consumed by green crabs and dogwhelks in this study. Figure A5 depicts the mean size

of mussels eaten by crabs only in treatment 2 and treatment 3. The difference between prey

size selection by crabs was not significantly different for the two types of predator systems

(t=0.627, p-value=0.543).

4. Discussion

4.1 Prey Consumption – Dogwhelk Predators

Mussel consumption was significantly lower for whelks in mixed-predator treatments

relative to the whelk-only treatments. Previous research supports the diminished response of

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whelk feeding rates in the presence of crabs. Lab studies conducted by d’Entremont (2005) and

Trussel et al. (2003) observed a reduction in feeding activity by dogwhelks when they were

exposed to crab risk cues. d’Entremont (2005) also tested whelk feeding rates in the field and

similarly found a decrease in consumption when predatory crabs are within the same

environment. He explains that physical disturbance by foraging crabs and potential for

intraguild predation serves to intensify feeding inhibition of whelks, as they often seek shelter

when crab risk cues are detected from the surrounding seawater (d’Entremont, 2005).

In whelk-only treatments, the mean consumption of mussels was significantly higher.

Previous research on the effects of whelk feeding by intraspecific competitive have been

inconsistent. Hughes and Dunkin (1984) proposed that whelks are stimulated to increase

consumption rates due to the scent of feeding conspecifics. Within the lab, d’Entremont (2005)

also found a slight positive stimulatory effect of foraging conspecifics on whelk feeding activity.

Intraspecific competition can also be negative between whelks, where they can engage in

interference competition by displacing each other from mussel prey or kleptoparasitism

(Hughes and Dunkin, 1984).

Both interspecific and intraspecific interactions have the potential to decrease feeding

activity of whelks. Consumption was significantly higher in whelk-only treatments, therefore it

is suggested that multiple-predator interactions and crab risk cues have a stronger influence on

whelk foraging rate.

4.2 Prey Consumption – Crab Predators

Crab consumption of mussels was higher in multiple-predator systems where both crabs

and whelks were present. Previous studies have found a similar positive interaction between

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green crabs and dogwhelks. An increase in biomass consumed by crabs when competing for

food with dogwhelks was found by Quinn (2010), suggesting that whelks have the ability to

facilitate crab feeding rates possibly through kleptoparasitism. Kleptoparasitism is a form of

exploitative competition that involves the theft of a food item already acquired by another

organism (Smalegange et al., 2006). In the present study, out of 8 experimental trials

amounting to a total of 96 hours, only one mussel was consumed by whelks when both

predators were present in the foraging area. On the contrary, in 8 trials a total of 31 mussels

were consumed by green crabs when both predators were present. Although no video

evidence was recorded, it is possible that the high number of mussels consumed by crabs were

due to kleptoparasitic activities on whelks. Crabs can detect chemical cues in the water to

initiate kleptoparasitic attacks, since the drilling of a dogwhelk cause a surge of chemicals and

other stimuli to be released from the prey (Smalegange et al., 2006). The process of whelk

consumption of mussels also weakens the structure of the shell and strength of the adductor

muscle, which allows crabs to exploit the weakened prey and reduce handling time (Crothers,

1985).

In addition to crabs stealing food from whelks, crabs also occasionally consume whelks

in order to decrease interspecific competition for limited food resources (d’Entremont, 2005).

Three whelks were consumed by crabs in treatment 2 of this study out of a possible 56 whelk

individuals in all 8 trials. Green crab consumption of dogwhelks is a form on intraguild

predation, which renders the net effect of two predators to be less than additive (d’Entremont,

2005; Sih et al., 1998). From analysis of treatment 2 results, it is evident that the presence of

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whelks had a positive effect on crab foraging. The ability for whelks to facilitate feeding of

crabs may have moderated the negative effects of intraspecific competition between crabs.

Lower mussel consumption was found for green crabs experiencing only intraspecific

competition. Foraging depression of crabs was found in previous studies in which aggressive

behaviour and interference competition between conspecifics inhibited feeding (Griffen and

Williamson 2008; Rovero et al., 2000; Quinn et al., 2012). Only 19 mussels were consumed by

crabs in treatment 3, experiencing only intraspecific competition for prey. In a study conducted

by Quinn (2010), crabs were found to consume less biomass when found in high crab densities,

which was suggested to be a result of antagonistic interactions. Smallegange et al. (2006) also

suggests that green crabs in high densities have a reduction in feeding rates due to interference

competition. They observed an increase in handling time due to intraspecific competition,

possibly due to the crabs being more vigilant and aggressive.

4.3 Size Selection of Prey

Green crabs and dogwhelks have a preferred size range of prey, which is related to crab

carapace width and whelk shell height (Hughes and Dunkin, 1984). In stressful environments,

such as high species density, times of starvation, or competitive interactions between

predators, species can adjust their preferred range of mussel prey (Rovero et al., 2000).

Crab sizes were within a range of 48-68mm in carapace width. Dogwhelks ranged from

25-40mm in height. Mussels were collected and ranged in size from 30-50mm. Smaller

mussels are usually preferred by crabs because it requires less energy to acquire food, however

preferred size classes often become depleted and crabs must be flexible in selecting larger prey

(Hughes and Dunkin, 1984). Larger crabs were used in this study and according to Quinn

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(2010); prey size flexibility is more possible for larger crabs because the maximum size those

individuals can consume increases with body size. As a result, crabs in this study did not have

to be selective about which mussels they consumed because all mussels used were within the

range of possible consumption. Dogwhelks can consume mussels up to 50mm in length (Quinn

2010). Whelks used in this study were not-size selective because they could consume all

mussels provided in the tanks. Prey size selection was not significantly different for green crabs

and dogwhelks across all treatments. This may be due to the fact that crab risk cues nearly

eliminated mussel consumption by whelks in multiple-predator treatments, and therefore

whelks or crabs did not pressure each other to alter their prey size selection.

Sizes of mussels consumed by crab predators were not statistically different for multiple

and single predator treatments. However, the average size of mussels consumed by crabs in

the presence of whelks was higher than those consumed in crab-only treatments. Larger

mussels require longer handling times, so kleptoparasitism may be beneficial as it lowers

handling time and increases the biomass returned (Iyengar, 2008). In mixed-predator

treatments, any kleptoparasitism of mussels being eaten by whelks that occurred may have

facilitated consumption of larger mussels by crabs.

4.4 Conclusions

The effects of intra- and interspecific interactions between predators of blue mussels

appear to play an important role in community dynamics. Whelks appear to engage in positive

intraspecific interactions in which feeding by conspecifics stimulates whelk foraging activities.

Both intraspecific and interspecific interactions have the potential to reduce feeding activity of

whelks. Consumption was significantly higher in whelk-only treatments, therefore it is

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suggested that interspecific competition and crab risk cues have a stronger influence on

decreasing whelk foraging rates. Crabs consumed more mussels when whelks were present,

suggesting that whelks have the ability to facilitate crab feeding rates possibly through

kleptoparasitism. Future research should focus on the importance and frequency of

kleptoparasitism between different sizes of predators, other predators influencing the

interactions between whelks and crabs, and the long-term consequences of decreased feeding

of dogwhelks in the presence of green crabs.

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17 | R . B r o d i e / P r e d a t o r i n t e r a c ti o n s b e t w e e n g r e e n c r a b s a n d d o g w h e l k s i n t h e p r e s e n c e o f b l u e m u s s e l p r e y

Appendix Aa)

1 2 30

0.5

1

1.5

2

2.5

3

3.5

4

4.5

Treatment

a

b

b)

1 2 30

0.5

1

1.5

2

2.5

3

3.5

4

4.5

5

Consumed by WhelkConsumed by Crab

Treatment

Figure A1. Mean consumption of mussels over a 12 hour period by a) all predators collectively in the foraging environment and b) each individual species. Treatment 1 consists of dogwhelks predators, treatment 2 consists of crab and whelk predators, and treatment 3 has crab predators. In figure A1a) A significant difference is observed for treatment 2, where a higher number of mussels are consumed when both predators are present in the same environment (F = 7.982, MS = 12.875, df = 2, Tukey’s HSD test p-value = 0.003). Different letters on the graph A1a) indicate significant differences between the treatments. All species tested were collected from tide pools found in the intertidal zone of Indian Point, New Brunswick.

a

Mean Number of Mussels Consumed over a 12 hour period

18 | R . B r o d i e / P r e d a t o r i n t e r a c ti o n s b e t w e e n g r e e n c r a b s a n d d o g w h e l k s i n t h e p r e s e n c e o f b l u e m u s s e l p r e y

1 20

0.2

0.4

0.6

0.8

1

1.2

1.4

1.6

Treatment

Mea

n N

umbe

r of M

usse

ls Co

nsum

ed o

ver a

12

hour

pe

riod

Figure A2. Mean number of mussels consumed by whelks when no crabs are present (treatment 1) in comparison to consumption by whelks in the presence of crabs (treatment 2). Averages were taken from 8 different trials, each with duration of 12 hours. Mussels consumed by whelks in treatment 1 is significantly higher than mussels eaten by whelks in treatment 2 (x2 = 9.734, df = 1, p-value = 0.002). All species tested were collected from tide pools found in the intertidal zone of Indian Point, New Brunswick.

a

b

19 | R . B r o d i e / P r e d a t o r i n t e r a c ti o n s b e t w e e n g r e e n c r a b s a n d d o g w h e l k s i n t h e p r e s e n c e o f b l u e m u s s e l p r e y

2 30

0.5

1

1.5

2

2.5

3

3.5

4

4.5

Treatment

Mea

n N

umbe

r of M

usse

ls Co

nsum

ed o

ver a

12

hour

per

iod

a

Figure A3. Mean number of mussels consumed by crabs when whelks are present (treatment 2) in comparison to consumption by crabs when whelks are not present (treatment 3). Averages were taken from 8 different trials, each with duration of 12 hours. The difference between mussels consumed by crabs in the presence of whelks and absence of whelks is approaching significance (t = 2.093, df = 13.217, p-value = 0.056). All species tested were collected from tide pools found in the intertidal zone of Indian Point, New Brunswick.

ab

20 | R . B r o d i e / P r e d a t o r i n t e r a c ti o n s b e t w e e n g r e e n c r a b s a n d d o g w h e l k s i n t h e p r e s e n c e o f b l u e m u s s e l p r e y

1 2 341

42

43

44

45

46

47

48

Treatment

Mea

n siz

e of

mus

sels

cons

umed

(mm

)

a

Figure A4. Mean size of mussels consumed (mm) over a 12 hour period for each treatment. Treatment 1 consists of conspecific dogwhelk predators, treatment 2 consists of crab and whelk predators, and treatment 3 has conspecific crab predators. The mean size of mussels consumed by whelks in treatment 1 is higher than all other treatments, but this is not statistically significant (F= 1.664, df = 2, p-value = 0.215). All species tested were collected from tide pools found in the intertidal zone of Indian Point, New Brunswick.

a

a

21 | R . B r o d i e / P r e d a t o r i n t e r a c ti o n s b e t w e e n g r e e n c r a b s a n d d o g w h e l k s i n t h e p r e s e n c e o f b l u e m u s s e l p r e y

2 342

42.5

43

43.5

44

44.5

Treatment

Mea

n Si

ze o

f Mus

sels

Cons

umed

(mm

)

Figure A5. Mean size of mussels consumed (mm) over a 12 hour period by crabs when whelks are present (treatment 2) in comparison to consumption by crabs when whelks are not present (treatment 3). Crabs in treatment 2 consumed mussels that were of a larger mean size, but this is not statistically significant (t = 0.627, df = 11.318, p-value = 0.543). All species tested were collected from tide pools found in the intertidal zone of Indian Point, New Brunswick.

a

a