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Journal of Experimental Marine Biology and Ecology 506 (2018) 30-41 



ELSEVIER 


Contents lists available at ScienceDirect 

Journal of Experimental Marine Biology and Ecology 

journal homepage: www.elsevier.com/locate/jembe 



What happens after mussels die? Biogenic legacy effects on community 
structure and ecosystem processes^ c ^ r 

John A. Commito a,b ’*, Brittany R. Jones a<1 , Mitchell A. Jones 3 , Sondra E. Winders 3 , Serena Como c 

a Environmental Studies Department, Gettysburg College, Gettysburg, PA 17325, USA 

b Unita di Biologia Marina ed Ecologia, Dipartimento di Biologia, Universita di Pisa, Via Dema 1, 56126 Pisa, Italy 

c Consiglio Nazionale delle Ricerche, Istituto per VAmbiente Marino Costiero (CNR-IAMC), Localitd Sa Mardini, Torregrande 09170, Oristano, Italy 


ARTICLE INFO 


ABSTRACT 


Keywords: 

Ecosystem engineer 
Legacy effects 
Mussel bed 
Mytilus edulis 
Shell hash 
Soft-bottom 


Mussels are well-known ecosystem engineers in soft-bottom systems. Mytilus edulis beds have myriad effects on 
sediment, benthic organisms, and ecosystem processes such as hydrodynamic transport of sediment and animals. 
When mussels die, they may leave behind massive amounts of whole (empty) and fragmented shells. The legacy 
effects of this long-lasting biogenic material (i.e., shell hash) on benthic systems are poorly understood. We 
measured percent cover values of 4 bottom cover types, i.e., live mussels, whole shells, fragmented shells, and 
bare sediment, at the mussel bed in Carrying Place Cove, Harrington, Maine, USA, and examined their effects on 
sediment characteristics, community structure of macrofauna and meiofauna, and ecosystem processes of se¬ 
diment flux and dispersal of postlarval macrofauna and meiofauna. We predicted that live mussels are the cover 
type with the greatest effects compared to bare sediment, followed by fragmented shells and then whole shells. 
We discovered mostly bare sediment, substantial cover of whole and fragmented shells, and almost no live 
mussels in what had in past years been a robust bed. We found significant univariate and multivariate differences 
in sediment and animals across cover types, especially for meiofauna. Fragmented shell material in particular 
may be an important driver in this system. Our results are the first to quantify the 4 mussel bed cover types and 
demonstrate their effects. Mussel beds in the Gulf of Maine have experienced severe declines in the past two 
decades, attributed primarily to climate change and the invasive green crab, Carcinus maenas. Our results may be 
useful in predicting the responses of soft-bottom systems as intact mussel beds die off, leaving large areas of bare 
sediment and shell hash. 


1. Introduction 

Mussels are well-known ecosystem engineers in soft-bottom sys¬ 
tems. Blue mussel (Mytilus edulis ) beds have myriad effects on sediment, 
infauna, epifauna, and ecosystem processes like wind-generated bed¬ 
load transport and animal dispersal (Bouma et al., 2009; Buschbaum 
et al., 2009; Commito et al., 2005, 2008; Gutierrez et al., 2011). When 
soft-bodied ecosystem engineers such as polychaetes die, their impact 
may soon begin to wane (Gutierrez et al., 2011; Reise, 2002). But 
mussels and other hard-bodied ecosystem engineers may leave behind 
massive amounts of whole (empty) and fragmented shells (Fig. 1A; 
Commito et al., 2008, 2014). The legacy effects of this long-lasting 
biogenic material (i.e., shell hash) on community structure and eco¬ 
system processes are poorly understood. 


Mussel beds consist of intermingled patches of live mussels, bare 
sediment, and whole and fragmented shells (Fig. IB). Because beds in 
Maine have a hierarchical, fractal spatial structure down to the milli¬ 
meter scale (Snover and Commito, 1998; Commito and Rusignuolo, 
2000; Commito et al., 2016), even a small mussel bed patch may consist 
of smaller patches of all 4 components. Moreover, live mussels attach to 
each other and to whole and fragmented shells, bound together by 
byssal threads. Thus, ecosystem engineering effects of mussel beds 
cannot be attributed solely to the live mussel component. Yet to our 
knowledge, no study of the effects of mussel shell hash has ever been 
conducted at an intertidal, soft-bottom mussel bed anywhere in the 
world. 

Mollusk shell material can have important impacts on habitat pro¬ 
vision, water flow, recruitment, food supply, predation, and other 


^ Author contribution: JAC, BRJ, MAJ, and SC conceived and designed the field work. JAC, BRJ, and MAJ carried out the field work. JAC, BRJ, MAJ, and SEW carried out the 
laboratory work. JAC, BRJ, MAJ, SEW, and SC analyzed the data and wrote the manuscript. 

* Corresponding author at: Environmental Studies Department, Gettysburg College, Gettysburg, PA 17325, USA. 

E-mail address: jcommito@gettysburg.edu (J.A. Commito). 

1 Present address: College of Fisheries and Ocean Sciences, University of Alaska Fairbanks, Fairbanks, AK 99775, USA. 

https://doi.org/10.1016/jjembe.2018.05.004 

Received 22 August 2017; Received in revised form 11 May 2018; Accepted 12 May 2018 

Available online 25 May 2018 

0022-0981/ © 2018 Elsevier B.V. All rights reserved. 




















J.A. Commito et al 


Journal of Experimental Marine Biology and Ecology 506 (2018) 30-41 



B 

Live mussels Whole shells 


Fragmented shells Bare sediment 


Fig. 1. Mussel bed bottom cover. (A) Shell hash at our mussel bed study site: 
Carrying Place Cove, Harrington, Maine, USA. (B) Types of bottom cover found 
in Maine mussel beds. 


Patch attribute Strength of effects on benthic systems 

Weak Strong 

Size 


Age 


Vertical dimension 


Surface topography 


Mobility of components 


Porosity (gap widths) 


Production of materials 
(e.g., feces, pseudofeces) 

Percent cover 


Areal extent 


Fig. 2. Mussel bed patch characteristics. Attributes presented across the range 
from weak to strong effects on soft-bottom sediment, community structure, and 
ecosystem processes of sediment flux and animal transport in bedload. 

factors (Gutierrez et al., 2003, 2011), often causing an increase in in¬ 
fauna, epifauna, and species diversity in benthic systems (Guay and 
Himmelman, 2004; Gutierrez et al., 2003; Hily, 1991; Hubbard, 2016; 
Kraeuter et al., 2003; Ribeiro et al., 2005; Rodney and Paynter, 2006; 
Summerhayes et al., 2009; Tomatsuri and Ron, 2017; Wilding and 
Nickell, 2013). However, some studies have found mixed, weak, or no 
significant effects (Bomkamp et al., 2004; Gutierrez and Iribarne, 1999; 
Hewitt et al., 2005; Mann et al., 2016; Nicastro et al., 2009; Turner 
et al., 1997). The wide-ranging responses to living bivalves and non¬ 
living biogenic structure make it difficult to predict the expected 
magnitude and even the direction of differences among live mussels, 
whole shells, and fragmented shells relative to bare sediment. The im¬ 
pacts most likely stem from variations in bed patch attributes such as 
those presented in Fig. 2. 

It seems plausible that effects on ambient sediment and organisms, 
as well as on flow-related sediment flux and animal transport, are 


JM* 


Large 






Thick, deep 




w Smooth 

Rough 


Easily transported Stationary 







Open (wide) 

Closed (narrow) 





J— 



Shell hash 

Live mussels 




— ■ —,-^ ^ 



Low 

High 



* 

w v 

yf- It) .#!■* 


Small 

Large 


greatest for live mussels, followed by fragmented shells and then whole 
shells. We make this prediction because live mussels produce copious 
amounts of feces and pseudofeces that increase the silt-clay fraction and 
create low-oxygen, high sulfide conditions that are detrimental to most 
species but favorable to a few others, e.g., the oligochaete Tubificoides 
benedeni and opportunistic polychaetes like Capitella capitata (Albrecht 
and Reise, 1994, Albrecht, 1998; Commito et al., 2005, 2008; Kent 
et al., 2017; Ragnarsson and Raffaelli, 1999). In addition, live mussels 
project up into the water column above the bottom, and this roughness 
profile has strong effects on flow dynamics that increase the capture of 
sediment, postlarval macrofauna, and meiofauna moving across the 
bottom (Commito and Rusignuolo, 2000; Commito et al., 2005). 

Fragmented shells may be next in importance because they can 
often be observed in dense, tightly packed patches that may act as a 
barrier between the sediment and the water column. Packing theory 
demonstrates clearly that packing is tighter, with lower porosity, when 
the objects are of many sizes, allowing small ones to fill in the gaps 
between large ones (Chen et al., 2003). Thus, at our sites in Maine we 
observe that fragmented shell pieces, which exist in angular shapes of 
all sizes, are generally more tightly packed than whole shells. Frag¬ 
mented shells also alter sediment structure by contributing directly to 
the coarse sediment fraction. Species abundances in Maine mussel beds 
can be positively or negatively correlated with coarse, terrestrially-de¬ 
rived gravel (Commito et al., 2008), so they may respond similarly to 
coarse, fragmented shell material as well. In particular, fragmented 
shells might be expected to depress animal abundance by blocking the 
movement of oxygen into the sediment below. Their influence on flow 
dynamics, hence the movement of sediment and animals, is probably 
less than that of live mussels because fragments do not project as high 
up into the water column. 

Whole shells are often loosely packed. They are generally larger 
than fragments, and their large-radius curves leave sizable gaps be¬ 
tween neighboring shells even when touching because they have no 
straight, parallel sides. This porosity due to gaps within a patch may 
create less of a sediment-water column barrier compared to fragmented 
shell cover. We also observe that whole shells tend to lie flat on the 
bottom, often concave-side down, presenting a relatively smooth bed 
surface that may not induce as much turbulent flow as does a bed with 
the rough topography of live mussels or fragmented shell pieces. Thus 
we expect whole shells to have less of an impact on sediment, animals, 
and hydrodynamics than do live mussels and fragmented shells. 

In this study we investigated biogenic legacy effects by comparing 
sediment characteristics, community structure of macrofauna and 
meiofauna, and the ecosystem processes of sediment flux and faunal 
transport in isolated patches of live mussels, bare sediment, whole 
shells, and fragmented shells in a Maine soft-bottom mussel bed. Mussel 
beds in the Gulf of Maine have recently experienced severe declines, 
with reduced larval settlement and decimated abundances of juveniles 
and adults in the past two decades (Petraitis and Dudgeon, 2015; Sorte 
et al., 2011, 2016). The bottom cover proportions of whole shells, 
fragmented shells, and bare sediment may be increasing relative to that 
of live mussels. If so, our results could be useful in understanding how 
soft-bottom systems respond to the apparent mussel bed decline. 

2. Methods 

2.1. Study site 

The research was conducted at the intertidal, soft-bottom Mytilus 
edulis bed in Carrying Place Cove, Harrington, Maine, USA (44.5451°N, 
— 67.7844°W), a relatively protected embayment with a bottom of 
muddy sand (Fig. 3). As is typical in this region, the bed extends across 
the mouth of the cove near the low tide line. The ecology of eastern 
Maine soft-bottom mussel beds like this one has been well studied, 
including their spatial abundance patterns (Commito et al., 2006, 2014; 
Crawford et al., 2006), sediment and macrofauna (Commito et al.. 


31 






















































































J.A. Commito et al. 


Journal of Experimental Marine Biology and Ecology 506 (2018) 30-41 



Fig. 3. (A) Location of study site in eastern Maine, USA. (B) Aerial view of Carrying Place Cove, Harrington, Maine, with mussel bed and transects indicated. Cores 
were taken and traps deployed immediately south of Transect C. Map data copyright 2015 Google. 


2005, 2008), and impacts on sediment flux and postlarval dispersal 
dynamics (Commito et al., 2005). The intertidal, soft-bottom mussel 
beds in eastern Maine that we have studied for decades typically had = 
50% cover of live mussels in complex fractal power-law spatial patterns 
(Commito et al., 2006, 2014; Crawford et al., 2006). The remaining bed 
surface consisted primarily of bare sediment with small percent cover 
values of whole (empty) mussel valves and mussel shell fragments. 
Today, some of the largest, densest beds where we have conducted 
research since the mid-1970s contain virtually no live mussels (John A. 
Commito, personal observation; Brian F. Beal, personal communica¬ 
tion). Our original intent was to conduct this investigation at the nearby 
Guard Point mussel bed because we had results from past studies there 
for possible comparison (Commito et al., 2005, 2006, 2014). However, 
we could not locate any live mussels except for some scattered in¬ 
dividual on this once thriving bed, requiring us to move = 1 km to 
Carrying Place Cove, which has similar sediment and other character¬ 
istics. No long-term time series of aerial photographs suitable for mussel 
cover analysis exists for Carrying Place Cove. However, our field ob¬ 
servations at the site over the last 30 years suggest that mussel abun¬ 
dance at Carrying Place Cove has dropped precipitously, resulting in a 
scattered array of small, isolated patches of live mussels in a complex 
pattern with bare sediment, whole mussel shells, and mussel shell 
fragments over the bed surface (Fig. 1A). 

In this project we used photo transects to quantify the percent cover 
of each of the 4 cover types: live mussels, whole mussel shells, frag¬ 
mented mussel shells, and bare sediment. In patches of each cover type, 
we used: (1) core samples to compare univariate and multivariate 
measures of sediment characteristics, macrofauna, and meiofauna; and 
(2) bottom traps to compare the ecosystem processes of sediment flux 
and dispersal of postlarval macrofauna and meiofauna. 

2.2. Cover types 

Digital photographs were taken every meter along 3 transects 
(Transect C on 4 August 2011, Transects A and B on 31 July 2012) that 
ran from the upper to the lower margin of the mussel bed (Fig. 3). No 
transects were established in the southern portion of the bed because of 
possible effects on the bottom in that area from occasional light activity 
by small boats. Images were cropped to an area of 0.25 m 2 . They were 
uploaded into ArcMap and hand digitized into the 4 cover types (live 
mussels, whole shells, fragmented shells, and bare sediment). Percent 
cover of each cover type was determined using pixel counts. Transect 


results were plotted with a 3-cell running average for smoothing. 

2.3. Ambient sediment, macrofauna, and meiofauna 

We followed Hurlburt's (1984) recommendations for treatment in- 
terspersion when spatial heterogeneity is expected, particularly in field 
projects of this size. Our sample design utilized his systematic model to 
achieve treatment interspersion, reducing the likelihood of treatment 
segregation, type 1 error, and spurious treatment effects. Our goal had 
been to sample large patches similar in size to those from a previous 
study at Guard Point, where we were able to select live mussel patches 
> 6.0 m in the smallest dimension (Commito et al., 2005). Although we 
commonly observed such large patches in past years at Carrying Place 
Cove, none approaching that size could be found at the time of this 
study. Live mussel patches were smaller and far less common than the 
other 3 cover types, so we searched for live mussels and chose the 10 
mussel patches >0.5m x 0.5 m in size nearest to Transect C within 
a = 10 m wide band from the upper to the lower mussel bed margin (~ 
100 m). We then selected the patches >0.5m x 0.5 m of each of the 
other 3 cover types closest to each live mussel patch. Thus, N = 10 for 
each of the 4 cover types. 

At low tide on 15 May 2011, 1.3 cm diameter cores (cross-sectional 
area = 1.33 cm 2 ) were taken to a depth of 5 cm at the 40 sampling 
locations. Cores of this size were used successfully to sample sediment 
characteristics, macrofauna, and meiofauna at similar sites nearby, 
collecting approximately the same numbers of macrofaunal species as 
larger cores and allowing us to utilize a larger sample size with the 
same sampling and laboratory processing effort (Commito and Tita, 
2002; Commito et al., 2005, 2008). Core contents were stained with 
rose bengal and fixed in situ with buffered formalin. In the laboratory, 
samples were wet sieved on 0.5 mm (to obtain macrofauna and the 
coarse sediment fraction) and 0.063 mm (meiofauna and fine sediment 
fraction) mesh, and the material that passed through the sieves (silt- 
clay sediment fraction) was retained. Macrofauna (to species level when 
possible, using Pollock, 1998) and meiofauna (to family or higher le¬ 
vels, e.g., Copepoda, Nematoda, Foraminifera) were identified and 
counted in gridded Petri dishes. The 3 sediment size-classes were dried 
at 85 °C for 24 h and weighed. Organic matter was calculated using loss- 
on-ignition by burning at 500 °C for 4h (Dean, 1974). 


32 













J.A. Commito et al 


Journal of Experimental Marine Biology and Ecology 506 (2018) 30-41 


<D 

> 

O 

O 


0 

Q. 


0 

> 

O 

O 



0 50 




Distance from upper to lower mussel bed margin (m) 


Fig. 4. Percent cover values for cover types along transects. Note different 
transect lengths on horizontal axes. See Table 1 for summary values. 


2.4. Sediment flux and animal dispersal as ecosystem processes 

On 15 May 2011, 15.0 cm tall bottom traps of the same diameter as 
the coring device (aspect ratio = 11.5:1) were filled with seawater and 
inserted flush with the sediment surface into the holes created during 
the core sampling described above. Traps of this design were used 
successfully to measure sediment flux and dispersal of macrofauna and 
meiofauna at similar sites nearby (Commito and Tita, 2002; Commito 
et al., 2005). To assure that the traps did not lose their capture effi¬ 
ciency by filling with sediment and effectively lowering their aspect 
ratio, they were removed and replaced with new traps inserted into the 
same holes at low tide on each of the following 3 days. Trap samples 
were processed in the same way as the cores. Data from the daily trap 
contents were combined to create a cumulative sample for the 3 day 
deployment period. Following Commito et al. (1995a, 2005) and 
Commito and Tita (2002), the sediment flux rate = g sediment trap -1 
deployment -1 and the animal dispersal rate = number of individuals 
trap -1 deployment -1 were calculated. Despite being marked with 
flags, some traps were impossible to locate due to burial by shell hash 
moved by water currents. Because our multivariate statistical approach 
(see below) required a balanced design, trap samples from each cover 
type were eliminated at random to achieve an equal number of re¬ 
plicates (IV = 8) for each cover type. 

2.5. Data analysis 

Analysis of the cores and traps included the sediment mass in each 
size-class (silt-clay, fine sand, coarse material) and percent organic 
matter, as well as the total abundance, species richness, Shannon- 
Wiener Index (H') using log base e, and abundance of each dominant 
taxon in the macrofauna and meiofauna, respectively. Because the 


oligochaete Tubiflcoides benedeni often dominates the macrofauna in 
mussel beds and exhibits abundance patterns different from other 
macrofaunal species (Commito et al., 2005, 2008), the non-oligochaetes 
were also analyzed together as one group. 

For each core and trap variable, differences among cover types (4 
levels: fixed) were analyzed with a 1-factor ANOVA. Homogeneity of 
variances was checked using Cochran's C-test, and, when necessary, 
data were transformed to reduce heterogeneity to acceptable levels, as 
indicated in the ANOVA tables. In these cases, back-transformed means 
and 95% confidence intervals were calculated. When significant dif¬ 
ferences among cover types were found (alpha = 0.05), a posteriori 
comparisons were made using SNK tests. Cases occurred where SNK 
could not discriminate among alternative hypotheses despite the sig¬ 
nificant ANOVA differences. Because a posteriori multiple comparisons 
have less power than the original ANOVA F-test, such cases indicated 
that the 2 cover types with the largest and smallest means were sig¬ 
nificantly different, and no further resolution among cover types could 
be determined (Underwood, 1997). All analyses were done with the 
GMAV 5 computer program (A. J. Underwood and M. G. Chapman, 
unpublished). 

For macrofauna and meiofauna in the ambient community and 
dispersing assemblages, differences among cover types (4 levels: fixed) 
were analyzed with a distance-based permutational multivariable 
analysis of variance (PERMANOVA) based on Bray-Curtis dissimilarity 
measures (Anderson, 2001; McArdle and Anderson, 2001). Raw, square 
root transformed, and presence/absence data were used in the analysis. 
Results were the same for all 3, so only results from raw data are pre¬ 
sented. PERMDISP was utilized to determine if significant PERMAN¬ 
OVA differences were due to cover type data dispersion or location in 
multivariate space (Anderson, 2006; Anderson et al., 2006). PERMA¬ 
NOVA and PERMDISP were executed using the functions “adonis” and 
“betadisper” in the “vegan” package for R v3.4.2 (R Core Development 
Team, 2015). The non-metric multidimensional scaling (nMDS) ordi¬ 
nation model based on the Bray-Curtis dissimilarity matrix was con¬ 
ducted with the PRIMER v5.2 package (Clarke and Warwick, 2001) to 
visualize cover type separation when PERMANOVA differences were 
significant. 


3. Results 

3.1. Cover types 

The 3 transects revealed consistent trends from the upper margin to 
the lower margin of the mussel bed (Fig. 4, Table 1). Live mussel cover 
was only 1-4% of the bed surface. A few individuals were found at the 
upper margin of the bed, but most were in the lower part of the bed 
near the low tide line. Whole shell cover (7-21%) and fragmented shell 
cover (4-15%) were much more extensive, particularly in the upper 
portion of the bed. Bare sediment (62-88%) was by far the largest cover 
type, especially in the middle and low portions of the bed. 


Table 1 

Cover values for 3 transects at Carrying Place Cove. Values may not add up to 
100% due to rounding. Transects extended from the upper margin to the lower 
margin of the mussel bed. See Fig. 3 for aerial view of the cove and Fig. 4 for 
transect details. 


Transect 

Length (m) 

Cover (%) 






Live 

Whole 

Fragmented 

Bare 



mussels 

shells 

shells 

sediment 

A 

76 

1.5 

21.3 

15.2 

61.8 

B 

107 

0.7 

6.6 

4.0 

88.7 

C 

112 

3.7 

10.1 

10.4 

75.3 


33 














J.A. Commito et al 


Journal of Experimental Marine Biology and Ecology 506 (2018) 30-41 


Cores: Sediment 



Fig. 5. Sediment results for cores. (A) Mass values of silt-clay (light gray), fine 
sand (medium gray), and coarse material (dark gray). (B) Percent total organic 
matter (TOM). Values are mean ± 1 SE, except back-transformed mean and 
95% confidence interval for coarse material, which required transformation to 
meet ANOVA assumptions. Live = live mussels, Whole = whole shells. 
Frag = fragmented shells. Bare = bare sediment. See Results and Table 2 for 
statistical analysis. 

3.2. Ambient sediment, macrofauna, and meiofauna 

The silt-clay and coarse sediment size-classes were significantly 
different among cover types (Fig. 5, Table 2). Silt-clay mass was 


Table 2 

ANOVA results for ambient community cores. 


Parameter 

Transform 

$ 3,36 

P 

SNK 

Sediment 

Silt-clay (g) 


4.78 

0.005 

Bare > Whole = Live = Frag 

Fine sand (g) 


2.1 

0.117 


Coarse material (g) 

Ln(X + 1) 

5.51 

0.002 

Frag > Whole = Live = Bare 

Total organic matter 


1.47 

0.24 


(%) 





Macrofauna 

Number of species 


2.09 

0.119 


H' 


0.92 

0.439 


Total abundance 

Ln(X + 1) 

1.22 

0.318 


Oligochaetes 


1.89 

0.149 


N on-oligochaetes 

Ln(X + 1) 

1.73 

0.179 


Capitella capitata 

Ln(X + 1) 

3.34 

0.03 

NAH (Live > Frag) 

Meiofauna 

Number of taxa 


0.51 

0.678 


H' 


1.53 

0.223 


Total abundance 


4.21 

0.012 

NAH (Bare > Whole) 

Nematodes 


4.4 

0.01 

NAH (Bare > Whole) 

Copepods 


2.66 

0.065 


Foraminiferans 


2.35 

0.089 



Significant differences (P < 0.05) are in bold. For parameters with significant 
differences among cover types, the SNK results are presented. NAH = no al¬ 
ternative hypothesis; the 2 cover types with the largest and smallest means were 
significantly different, and no further resolution among cover types was pos¬ 
sible. Live = live mussels, Whole = whole shells, Frag = fragmented shells, 
Bare = bare sediment. 


significantly greater in cores from the bare sediment cover type than 
from the other cover types, which were not significantly different from 
each other. Coarse material mass was significantly greater in cores from 
the fragmented shell cover type than from other cover types, which 
were not significantly different from each other (Table 2). The per¬ 
centage of organic material did not vary significantly among cover 
types (Fig. 5, Table 2). 

Sixteen macrofaunal species were found (Appendix A), of which the 
most abundant was the oligochaete Tubificoides benedeni (74% of the 
total), followed by the polychaete Capitella capitata and much smaller 
numbers of the other species.No significant differences were found 
among cover types except for C. capitata abundance (Fig. 6, 
Table 2).The a posteriori comparison test could not discriminate among 
alternative hypotheses, indicating that C. capitata was significantly 
more abundant in live mussel cover than in fragmented shell cover, and 
no further resolution among cover types was possible (Table 2).At the 
multivariate level, PERMANOVA revealed no significant differences in 
macrofaunal community structure among cover types with or without 
oligochaetes (Table 3). 

Six meiofaunal taxa were found (Appendix A), of which the most 
abundant were nematodes (81% of the total), followed by copepods, 
foraminiferans, and much smaller numbers of the other taxa.Total 
abundance and nematode abundance were significantly different 
among cover types (Fig. 7, Table 2).In both cases the a posteriori 
comparison test could not discriminate among alternative hypotheses, 
indicating that total meiofauna and nematodes were significantly more 
abundant in bare sediment cover than in whole shell cover, and no 
further resolution among cover types was possible (Table 2).At the 
multivariate level, PERMANOVA revealed significant differences in 
meiofaunal community structure among cover types (Table 3), and 
nMDS plots showed separation among cover types (Fig. 8), consistent 
with the PERMDISP result of no significant data dispersion 
0*3,36 = 0.47, P = 0.74).Dissimilarity values were large for fragmented 
and whole shells compared to bare sediment and, to a lesser degree, live 
mussels, highlighting the impact of shell hash on meiofaunal commu¬ 
nity structure. 

3.3. Sediment flux and animal dispersal as ecosystem processes 

The silt-clay and coarse sediment size-classes collected by traps 
were significantly different among cover types (Fig. 9, Table 4). In both 
cases the a posteriori comparison test could not discriminate among 
alternative hypotheses, indicating that trap values were significantly 
higher for silt-clay in live mussel cover than fragmented shell cover and 
for coarse sediment in fragmented shell cover than live mussel cover, 
and no further resolution among cover types was possible (Table 4). 
Total sediment mass collected by traps was not significantly different 
among cover types (Table 4), nor was the percentage of organic ma¬ 
terial (Fig. 9, Table 4). 

Twenty-four macrofaunal species were found in traps, and the 
species ranks were different from those in the ambient community cores 
(Appendix A). The most abundant species was still Tubificoides benedeni, 
but dropping to 43% of the total, followed by smaller numbers of other 
species, with no species a clear co-dominant, including Capitella capi¬ 
tata. No significant differences were found for any macrofaunal species, 
total abundance, species richness, or H' (Fig. 10, Table 4). At the 
multivariate level, PERMANOVA revealed no significant differences in 
macrofaunal dispersal assemblage structure among cover types 
(Table 5). 

Eight meiofaunal taxa were found in traps, and the taxon ranks were 
different from those in cores, with a dramatic shift to copepods as the 
dominant taxon (54% of the total), followed by nematodes, for¬ 
aminiferans, and much smaller numbers of the other taxa (Appendix A). 
Total abundance was significantly lower in traps from fragmented shell 
cover than from other the cover types, which were not significantly 
different from each other (Fig. 11, Table 4). H' and the abundances of 


34 



































J.A. Commito et al 


Journal of Experimental Marine Biology and Ecology 506 (2018) 30-41 


Cores: Macrofauna 


Number of species H' 




Oligochaetes 



Non-oligochaetes 



Total abundance 



Live Whole Frag Bare Live Whole Frag Bare 


Live Whole Frag Bare 


Fig. 6. Macrofauna results for cores. Values are mean ± 1 SE for number of species, Shannon-Wiener diversity index (HO, and abundance of the dominant species 
(the oligochaete Tubificoides benedeni ), and back-transformed mean and 95% confidence interval for total abundance, the non-oligochaetes as a group, and the second 
most abundant species (the polychaete Capitella capitatd), which required transformation to meet ANOVA assumptions. Live = live mussels, Whole = whole shells, 
Frag = fragmented shells, Bare = bare sediment. See Results and Table 2 for statistical analysis. 


Table 3 

PERMANOVA results for ambient community cores. 

Parameter MS F 3.36 P 


Macrofauna 




All species 

3118.75 

0.24 

0.275 

Without oligochaetes 

5283.76 

1.44 

0.275 

Meiofauna 

3364.62 

2.48 

0.031 


Within cover type: 

Live = 43.53 
Whole = 49.23 
Frag = 49.61 
Bare = 39.91 
Among cover types: 
Live vs Whole = 48.88 
Live vs Frag = 48.24 
Live vs Bare = 42.67 
Whole vs Frag = 47.69 
Whole vs Bare — 54.22 
Frag vs Bare = 55.53 


Significant differences (P < 0.05) are in bold. For parameters with significant 
differences among cover types, the mean Bray-Curtis dissimilarity (%) values 
within and among cover types are presented. Live = live mussels, 
Whole = whole shells. Frag = fragmented shells, Bare = bare sediment. 

nematodes and foraminiferans also differed significantly among cover 
types (Fig. 11, Table 4). In all 3 cases the a posteriori comparison test 
could not discriminate among alternative hypotheses, indicating that 
trap values were significantly higher for H' in bare sediment than live 
mussels, nematodes in bare sediment than fragmented shells, and for¬ 
aminiferans in bare sediment than live mussels, and no further resolu¬ 
tion among cover types was possible (Table 4). At the multivariate 
level, PERMANOVA revealed significant differences in meiofaunal 
community structure among cover types (Table 5), and the nMDS plot 
showed separation among cover types (Fig. 8), consistent with the 


PERMDISP result of no significant data dispersion (F 3:28 = 0.97, 
P = 0.45). Dissimilarity values were large for fragmented shell cover 
compared to all the other cover types (Table 5), demonstrating its im¬ 
portant impact on the meiofaunal dispersal assemblage. 

4. Discussion 

4.1. Mussel bed cover 

The results presented here are the first to quantify live mussel, 
whole shell, fragmented shell, and bare sediment percent cover values 
and demonstrate effects of the 4 cover types. The mussel bed at 
Carrying Place Cove was primarily bare sediment, with substantial 
cover of whole shells and fragmented shells and almost no live mussels. 
The combined cover value of whole and fragmented shells was an order 
of magnitude larger than live mussel cover, revealing the importance of 
non-living biogenic material when considering the physical structure of 
this and probably other mussel beds. 

4.2. Does biogenic structure matter? 

The effects of mussel beds on sediment, ambient community, and 
ecosystem processes have been well studied in recent years (Bouma 
et al., 2009; Buschbaum et al., 2009; Commito et al., 2005, 2008, 2014; 
Gutierrez et al., 2011; Smith and Shackley, 2004; Thiel and Ullrich, 
2002). However, investigations have generally treated mussel beds as a 
single biotic unit, with little attempt at teasing apart the effects of their 
different structural components - live mussels, whole shells, and frag¬ 
mented shells - compared to bare sediment. 

We predicted that effects on ambient sediment and organisms, as 
well as on flow-related sediment flux and animal transport, are greatest 
for live mussels, followed by fragmented shells and then whole shells. 
We found significant differences across cover types at the univariate 


35 



























































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Journal of Experimental Marine Biology and Ecology 506 (2018) 30-41 


Cores: Meiofauna 


Number of species 




Copepods 



Total abundance 



Foraminiferans 



Live Whole Frag Bare Live Whole Frag Bare Live Whole Frag Bare 

Fig. 7. Meiofauna results for cores. Values are mean ± 1 SE for number of taxa, Shannon-Wiener diversity index (HO, total abundance, and abundances of the 
dominant taxa (nematodes, foraminiferans), and back-transformed mean and 95% confidence interval for the dominant taxon of copepods, which required trans¬ 
formation to meet ANOVA assumptions. Live = live mussels, Whole = whole shells, Frag = fragmented shells. Bare = bare sediment. See Results and Table 2 for 
statistical analysis. 


level in sediment structure and animal abundances for both the ambient 
community and the transported sediment and animals. The fragmented 
shell cover type was often most different from the others. We also found 
significant differences at the multivariate level for meiofauna in both 
ambient community and dispersing assemblage structure. The frag¬ 
mented shell cover type contributed most to the dissimilarity. Thus it 
seems that cover type is an important driver in mussel beds and that 
fragmented shell material may be particularly important. 

We studied patches >0.5 m x 0.5 m in size for all 4 cover types 
because we wanted all the patches to be similar in size, and live mussels 
were never observed in patches larger than this size. Most of our pat¬ 
ches were right at the lower size limit. Had we been able to use larger 
patches with lower perimeter: area ratios, it is possible that the influ¬ 
ence of cover type may have been stronger. Thus, our results are likely 
to be conservative estimates of cover type effects. 

4.2.1. Sediment 

Organic material in soft-bottom systems is typically linked posi¬ 
tively to the silt-clay fraction and negatively to the coarse fraction (Gray 
and Eliot, 2009). However, despite significant differences in the sedi¬ 
ment size-classes among cover types, with bare sediment cover having 
the most silt-clay and fragmented shell cover having the most coarse 
material, no significant differences occurred in the percentage of total 
organic material among cover types in cores or traps. This result was 
surprising because mussels produce feces and pseudofeces known to 
enhance local sedimentation and alter sediment structure (Albrecht and 
Reise, 1994, Albrecht, 1998; Commito et al., 2005; Kent et al., 2017; 
Ragnarsson and Raffaelli, 1999). However, it is possible that organi¬ 
cally rich feces and pseudofeces were exported from patches of live 
mussels to nearby patches of the other cover types, reducing differences 


in organic content (Donadi et al., 2013). 

Surface topography is generally roughest for live mussels, less rough 
for fragmented and then whole shells, and smoothest for bare sediment 
(Commito and Rusignuolo, 2000). These topographic differences shape 
hydrodynamic profiles because turbulence increases as a function of the 
roughness, number, and spacing of patches, as well as the amount of 
patch edge, with more turbulence at patch edges than at patch centers 
(Folkard and Gascoigne, 2009; Widdows et al., 2009). The result is 
generally more sediment erosion and resuspension due to higher tur¬ 
bulent kinetic energy and bed shear stress in patches of physical 
structure compared to bare sediment (wa Kangeri et al., 2016; Widdows 
et al., 2009), with increased sediment deposition in M. edulis beds 
(Albrecht and Reise, 1994; Albrecht, 1998; Commito et al., 2008; 
Ragnarsson and Raffaelli, 1999). Yet in this study we found no sig¬ 
nificant differences across cover types in total sediment collected by 
traps. One possible explanation is that the cover type patches were too 
small to produce an effect. Another possibility is that the differences in 
physical structure among the cover types, or even the presence of 
physical structure per se, were not enough to enhance sediment capture 
dramatically. In fact, the opposite may be true. A surface cover of gravel 
acts as “bed armor” that reduces bedload transport (Singer and 
Anderson, 1984). It is possible that live mussels, whole shells, and 
fragmented shells can also armor the surface, thus countering their 
effects as sedimentation-enhancing roughness elements. 

4.2.2. Macrofauna 

Our results revealed little difference in macrofauna among cover 
types. The only significant ANOVA difference was for the opportunistic 
polychaete Capitella capitata, the numerically dominant species. The 
ambiguous SNK result allowed the conclusion that its abundance was 


36 



































































J.A. Commito et al 


Journal of Experimental Marine Biology and Ecology 506 (2018) 30-41 


Meiofauna 




■ = Live mussels O = Fragmented shells 

O = Whole shells A = Bare sediment 

Fig. 8. Non-metric multi-dimensional scaling (nMDS) results for cases where 
PERMANOVA revealed significant differences among cover types. Meiofauana: 
(A) Cores, (B) Traps. No significant differences were observed for macrofauna. 

higher in live mussel cover than in fragmented shell cover. At the 
multivariate level, no significant differences were found among cover 
types. Numerous studies that have found higher total macrofaunal 
abundance in mussel beds compared to bare intertidal flats, probably 
due to the production of organically enriched, low oxygen, high sulfide 
sediment favorable to oligochaetes and opportunistic species like C. 
capitata, especially those without free-swimming larvae (Buschbaum 
et al., 2009; Commito et al., 2005, 2008; Gutierrez et al., 2011; 
Ysebaert et al., 2009). The lack of major differences in macrofauna 
among cover types in our study most likely reflects the similarities in 
sediment structure and organic material observed across cover types. 

With respect to the dispersing assemblage, macrofaunal abundances 
in traps are often positively correlated with sediment mass in traps 
because animals may be transported like passive sediment particles 
(Commito et al., 1995a, 1995b; 2008; Turner et al., 1997; Valanko 
et al., 2010a, 2010b). Thus, the lack of clear patterns among cover types 
for macrofaunal abundance in traps in our study is consistent with the 
lack of significant differences in total sediment captured by traps. 

Our trap results demonstrated that the mussel bed system is highly 
dynamic, suggesting a potential for change over time. Traps on average 
collected approximately the same number of macrofaunal individuals in 
the 3-day deployment as were found in ambient assemblage cores, in¬ 
dicating a turnover time of = 3 days, where turnover time = (no. in¬ 
dividuals per core) 4- (no. individuals per trap per deployment period). 
This value is within the range of 1.4-4.3 days at a nearby mussel bed in 


Traps: Sediment 



Live Whole Frag Bare 

Fig. 9. Sediment results for traps. (A) Mass values of silt-clay (light gray), fine 
sand (medium gray), and coarse material (dark gray). (B) Percent total organic 
matter (TOM). Values are mean ± 1 SE. Live = live mussels, Whole = whole 
shells, Frag = fragmented shells, Bare = bare sediment. See Results and Table 4 
for statistical analysis. 


Table 4 

ANOVA results for dispersal assemblage traps. 


Parameter 

Transform 

F 3,28 

P 

SNK 

Sediment 





Total (g) 


1.11 

0.361 


Silt-clay (g) 


5.12 

0.006 

NAH (Live > Frag) 

Fine sand (g) 


0.51 

0.676 


Coarse material (g) 


4.56 

0.01 

NAH (Frag > Live) 

Total organic 


0.25 

0.861 


matter (%) 





Macrofauna 





Number of species 


0.5 

0.688 


H' 


0.65 

0.591 


Total abundance 

Sqrt(X + 1) 

0.64 

0.595 


Oligochaetes 


1.15 

0.349 


Non-oligochaetes 

Ln(X + 1) 

0.16 

0.92 


Meiofauna 





Number of taxa 


0.64 

0.594 


H' 

Ln(X + 1) 

3.44 

0.03 

NAH (Bare > Live) 

Total abundance 

Ln(X + 1) 

3.3 

0.035 

Bare = Whole = Live < F rag 

Nematodes 

Ln(X + 1) 

3.47 

0.029 

NAH (Bare > Frag) 

Copepods 


1.86 

0.16 


Foraminiferans 


3.71 

0.023 

NAH (Bare > Live) 


Significant differences (P < 0.05) are in bold. For parameters with significant 
differences among cover types, the SNK results are presented. NAH = no al¬ 
ternative hypothesis; the 2 cover types with the largest and smallest means were 
significantly different, and no further resolution among cover types was pos¬ 
sible. Live = live mussels. Whole = whole shells. Frag = fragmented shells, 
Bare = bare sediment. 

Maine (Commito et al., 2005) and 2.5-33 days calculated from data in 
Valanko et al. (2010a, 2010b) for a shallow, non-tidal, subtidal site in 
the Baltic Sea. It is longer than the range of 0.5-1.1 days for a small 
bivalve (Gemma gemma ) at a sandflat in Virginia (Commito et al., 
1995a), most likely because the sandflat had high wind velocities, and 


37 





































J.A. Commito et al 


Journal of Experimental Marine Biology and Ecology 506 (2018) 30-41 


Traps: Macrofauna 


Number of species 


5 


2.5 


0 J——-l_l-l_l 

Oligochaetes 




H' Total abundance 




Non-oligochaetes 



Live Whole Frag Bare 


Live Whole Frag Bare 


Fig. 10. Macrofauna results for traps. Values are mean ± 1 SE for number of species, Shannon-Wiener diversity index (HO, and abundance of the dominant species 
(the oligochaete Tubificoides benedeni), and back-transformed mean and 95% confidence interval for total number of individuals and the non-oligochaetes as a group, 
which required transformation to meet ANOVA assumptions. Live = live mussels, Whole = whole shells, Frag = fragmented shells, Bare = bare sediment. See 
Results and Table 4 for statistical analysis. 


Table 5 

PERMANOVA results for dispersal assemblage traps. 

Parameter MS F 3i2 s P 


Macrofauna 




All species 

2854.10 

0.97 

0.522 

Without oligochaetes 

3466.50 

0.86 

0.68 

Meiofauna 

2273.29 

2.19 

0.043 


Within cover type: 

Live = 35.99 
Whole = 49.50 
Frag = 42.71 
Bare — 32.31 
Among cover types: 

Live vs Whole = 41.83 
Live vs Frag = 47.53 
Live vs Bare = 34.07 
Whole vs Frag = 48.02 
Whole vs Bare = 41.05 
Frag vs Bare = 48.12 

Significant differences (P < 0.05) are in bold. For parameters with significant 
differences among cover types, the mean Bray-Curtis dissimilarity (%) values 
within and among cover types are presented. Live = live mussels, 
Whole = whole shells. Frag = fragmented shells, Bare = bare sediment. 

bedload transport and benthic animal transport are positively related to 
wind-generated hydrodynamic forces (Commito et al., 1995a, 1995b; 
Turner et al., 1997; Valanko et al., 2010a, 2010b). 

Traps collected macrofauna in different proportions than were 
found in the ambient community cores. Tubificoides benedeni, the 
dominant macrofaunal species in the ambient community, was the most 
abundant macrofaunal species in traps but dropped substantially as a 
proportion of the total. Yet for macrofauna, ambient community 
structure seems to persist in soft-bottom systems, despite the daily 


transport across the bottom of organisms with a different species mix 
than in cores (Commito et al., 2005; Turner et al., 1997; Valanko et al., 
2010a, 2010b). In the face of potential forcing from dispersing organ¬ 
isms, the strength of this resistance to change is a ripe topic for re¬ 
search. 


4.2.3. Meiofauna 

Cover type had stronger effects on meiofauna than on macrofauna. 
Significant ANOVA differences were found for total meiofauna and the 
numerically dominant nematodes. The ambiguous SNK results allowed 
the conclusion that abundances for both parameters were higher in bare 
sediment cover than in whole shell cover. At the multivariate level, 
significant differences in meiofaunal community structure occurred 
among cover types. Dissimilarity values indicated that fragmented and 
whole shells had a large impact on the meiofauna community. Some 
live bivalves (e.g., Cerastoderma glaucum, Macoma balthica, Mya are- 
naria\ Urban-Malinga et al., 2016) are known to enhance nematode, 
copepod, and total abundance values. We did not find this effect for live 
M. edulis. 

With respect to the dispersing assemblage, cover type again had 
stronger effects on meiofauna than on macrofauna. ANOVA revealed 
significant differences in several parameters, and total abundance was 
significantly lower in fragmented shell cover than in the other cover 
types. One possible explanation is that fragmented shell cover acted as 
bed armor to reduce the erosion and capture of local, within-patch 
meiofauna, especially in comparison with bare sediment. 

Traps collected 2.3-fold more meiofaunal individuals than were in 
cores, indicating a turnover time of = 1.3 days, which is shorter than 
the 4-day turnover time for meiofauna at a nearby Maine mudflat 
(Commito and Tita, 2002), most likely because wind velocities were 
higher during this study. As with macrofauna, traps collected meio¬ 
faunal taxa in different rank order than were found in the ambient 


38 




























































J.A. Commito et al 


Journal of Experimental Marine Biology and Ecology 506 (2018) 30-41 


Traps: Meiofauna 


Number of species h' 



Total abundance 




Fig. 11. Meiofauna results for traps. Values are mean ± 1 SE for number of taxa and abundances of the dominant taxa (copepods, foraminiferans), and back- 
transformed mean and 95% confidence interval for Shannon-Wiener diversity index (FT'), total number of individuals, and the dominant taxon of nematodes, which 
required transformation to meet ANOVA assumptions. Live = live mussels, Whole = whole shells, Frag = fragmented shells, Bare = bare sediment. See Results and 
Table 4 for statistical analysis. 


community. The rank orders of the 2 dominant taxa in cores, nematodes 
and copepods, were reversed in traps, with copepods the most abundant 
taxon by a wide margin, as was also observed in traps at a nearby 
mudflat (Commito and Tita, 2002). This reversal indicates clearly that 
copepods and nematodes do not disperse in the same way, most likely 
because copepods can live close to the sediment-water interface and 
engage in active emergence from the bottom in response to flow 
(Commito and Tita, 2002; Pacheco et al., 2013). 

4.3. Implications for mussel bed decline 

A serious decline in the abundance of intertidal mussels over the 
past several decades has been documented in the Gulf of Maine, in¬ 
cluding larvae, juveniles, and adults (Petraitis and Dudgeon, 2015; 
Sorte et al., 2011, 2016). We have observed this decline in eastern 
Maine, where we have conducted mussel bed research since the mid- 
1970s. The intertidal, soft-bottom mussel beds in eastern Maine that we 
have studied over the years typically had ~ 50% cover of live mussels 
in complex fractal power-law spatial patterns (Crawford et al., 2006). 
Many formerly robust beds contain virtually no live mussels today 
(John A. Commito, personal observation; Brian F. Beal, personal com¬ 
munication). They now consist largely of bare sediment with patches of 
shell hash. 

Individual soft-bottom mussel beds can experience short-term po¬ 
pulation swings (Folmer et al., 2014; Khaitov and Lentsman, 2016; 
Nehls and Thiel, 1993). But the Gulf of Maine decline encompasses 
much broader spatial and temporal scales and is generally attributed to 
climate change (Helmuth et al., 2006; Jones et al., 2010; Lesser, 2016; 
Sorte et al., 2011, 2016) and predation by the invasive green crab, 
Carcinus maenas (Grosholz and Ruiz, 1996; Tan and Beal, 2015; 
Whitlow and Grabowski, 2012). The decline may also be related to 
long-term oscillating oceanographic conditions in the northwest 
Atlantic region (Beaugrand et al., 2008; Edwards et al., 2013; Greene 


et al., 2013). Thus it may be premature to state with certainty that a 
permanent Gulf of Maine regime shift is occurring. Regardless of the 
reasons behind the reduction in mussels, their decline means that 
bottom cover values of whole shells, fragmented shells, and bare sedi¬ 
ment are likely to be increasing relative to live mussels. To the degree 
that Carrying Place Cove may serve as a general model for a mussel bed 
that has suffered declines, our results can be useful in helping to predict 
the responses to these changes. 

As mussels die from causes that do not affect the shell directly, they 
produce an increase in whole shell cover, followed by breakdown into 
coarse fragmented shell pieces. Crushing and chipping predators like 
Carcinus maenas contribute directly to the production of coarse shell 
fragments (Tan and Beal, 2015). In addition, whole and fragmented 
shells held by mussel byssal threads (Commito et al., 2014) are released 
as mussels die. Moreover, in our study we found that coarse material 
was captured at higher rates in fragmented shell cover than in bare 
sediment, a form of positive feedback that may contribute to the 
maintenance of the fragmented shell cover type. Despite this increase in 
shell hash, our transect results showed that bare sediment by far com¬ 
prised the largest bottom cover area in the Carrying Place Cove mussel 
bed. This result suggests that shell material is probably being exported, 
buried, or broken down into fine particles. Interestingly, although we 
have observed changing relative values of each cover type at Carrying 
Place Cove over the past several decades, the boundaries of the mussel 
bed have remained stationary. Live mussels are still present at the upper 
(landward) and lower (seaward) margins of the bed. We observe some 
internal shifting of whole and fragmented material on a daily basis, 
apparently resulting in net transport to the upper part of the bed, as 
seen in Fig. 4. We can find windrows of whole and fragmented mussel 
shells along the shoreline above the mussel bed. But unlike storm-in¬ 
duced movement of empty snail shells described by Nicastro et al. 
(2009), relatively little mussel shell material at our site seems so far to 
have been exported outside of the original bed boundary, perhaps due 


39 




























































J.A. Commito et al. 


Journal of Experimental Marine Biology and Ecology 506 (2018) 30-41 


to its position in a sheltered embayment. 

Small patch size may be at least partly responsible for the relatively 
small differences we found across cover types for many parameters. 
Small patch size may be the norm as intact mussel beds die off and large 
patches of live mussels give way to small patches of live mussels, whole 
shells, and fragmented shells scattered within large areas of bare sedi¬ 
ment. Intact mussel beds and other bivalve reefs are important eco¬ 
system engineers and provide valuable ecosystem services (Borsje et al., 
2011; Bouma et al., 2009; Buschbaum et al., 2009; Commito et al., 
2005, 2008; Gutierrez et al., 2011; Koch et al., 2009; Palumbi et al., 
2009; Stone et al., 2005). If patches reach a small enough size, then a 
tipping point may be reached when the system is no longer a functional 
mussel bed. Then its ecosystem engineering effects will be gone, as will 
the ecosystem services it once provided. 

5. Conclusion 

M. edulis beds comprise a spatial mosaic of live mussels, whole 
shells, fragmented shells, and bare sediment. Sediment and benthic 
fauna differ among these cover types, as do their rates of movement in 
bedload. Particularly in regions such as the Gulf of Maine, where mussel 
beds may be declining in response to factors including climate change 
and invasive predators, consideration of these differences will lead to 
better understanding of the ecology of mussel beds and soft-bottom 
systems overall. 

Supplementary data to this article can be found online at https:// 
doi.org/10.1016/j.jembe.2018.05.004. 

Acknowledgments 

We thank Angela Commito and Ann Commito for assistance in the 
field and the University of Pisa and Gettysburg College for their sup¬ 
port. Seth Barker, Brian Beal, Tom Crawford, William DeVoe, Heidi 
Leighton, Denis Nault, and Ann Thayer provided useful information on 
the availability of aerial mussel bed images. Two anonymous reviewers 
made comments that significantly improved this paper. Our work was 
funded by grants from the Gettysburg College Research and 
Professional Development Program (JAC), Gettysburg College Senior 
Honors Research Program (BRJ, MAJ, SEW), and Howard Hughes 
Medical Institute undergraduate research program to Gettysburg 
College (52007540) (SEW). 

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