macrofaunal responses to pit–mound patch dynamics in an intertidal mudflat: local versus...

313 (2004) 297–315

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Macrofaunal responses to pit–mound patch dynamics

in an intertidal mudflat: local versus

patch-type effects

Roman N. Zajac*

Department of Biology and Environmental Science, University of New Haven, 300 Orange Avenue,

West Haven, CT 06516, USA

Received 16 March 2004; received in revised form 22 July 2004; accepted 16 August 2004

Abstract

Biogenic structures created via feeding activities have varying effects on soft sediment

communities, altering population dynamics, creating a temporal mosaic of successional patches,

and ultimately increasing variation at different spatial scales. This study focused on assessing

population responses to pits (P) and mounds (M) in an intertidal mudflat (River Plym, England) in

order to determine (a) how these structures (max size 1400 cm2), and their formation, affected

infauna and (b) to what extent local variations in ambient communities may have affected infaunal

responses. Densities in 0- and 1-week-old pits were significantly lower than in ambient and mound

areas for most of the dominant infauna over the study period. Abundances were higher in mounds for

some species and responses to both structures differed among juveniles and adults. Recovery to

ambient levels in P–M systems took about 3 weeks, although their physical characteristics only

lasted about 2 weeks. Correlations among ambient densities and adjacent P–M systems were mixed,

but suggested decoupling between local ambient and P–M dynamics for some taxa either in relation

to age of the patch and/or size of the individuals. At the community level, local differences appeared

to be a significant source of variation in new pits, but differences were swamped out when

recruitment was high. Differences were more evident in older P–M systems. These results show that

sources of local variation in infaunal dynamics can be attributed to a combination of small-scale

disturbance/recovery processes and spatially and temporally changing ambient conditions.

0022-0981/$ -

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Journal of Experimental Marine Biology and Ecology

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ress: [email protected].

R.N. Zajac / J. Exp. Mar. Biol. Ecol. 313 (2004) 297–315298

Identifying extant spatial and temporal small-scale variation can be a critical component of

understanding and interpreting larger-scale dynamics of soft-sediment systems.

D 2004 Elsevier B.V. All rights reserved.

Keywords: Colonization; Disturbance; Macrofauna; Mounds; Mudflat; Patch Dynamics; Pits

1. Introduction

Analyses of benthic populations and communities at multiple spatial scales have revealed

that, although significant amounts of variation can be associated with meso- and large scales

(~10’ s of m2 and greater), there often remains a relatively large amount of unexplained

variation that is potentially associated with smaller spatial scales (e.g. Hodda ,1990;

Morrisey et al., 1992; Zajac et al., 2003). Such observations may be due, in part, to inherent

limitations in analytical approaches such as analysis of variance, but other, perhaps more

robust, approaches such as geostatistics, regression and/or autocorrelation are also sensitive

to sampling density or processes that generate small-scale variability in habitat patch

structure across benthic landscapes (e.g. Ellis and Schneider, 1997; Hewitt et al., 1997;

Legendre et al. 1997; Cole et al., 2001). Understanding how the complex mix of biological,

physical and chemical factors that affect macrofauna interact to generate small-scale

variation may be critical in unraveling mechanisms controlling infaunal dynamics over

larger spatial scales. Additionally, such information can help in marine environmental

assessment by providing insights regarding how natural variation may interact with changes

due to perturbations and in extrapolating from small-scale experiments (Thrush et al., 2000).

Biogenic structures are common features of benthic landscapes (e.g. Hall et al., 1994)

that may be a significant source of small-scale spatial, and temporal, macrofaunal

variation. These include mounds created by burrowing and feeding, e.g. by callianassid

shrimp (Posey, 1986) and polychaetes (Weinberg, 1984), pits created by feeding activities

of a variety of animals including whales and walruses (Oliver and Slattery, 1985; Oliver et

al., 1985), rays (Thrush et al., 1991) and crabs (Hall et al., 1991), and a variety of other

surface features (e.g. Brenchley, 1981; Grant, 1983). These structures, and the activities

creating them, have been shown to have varied effects on infaunal communities. A review

of infaunal responses to biogenic disturbance patches created by organismal feeding

activities across a variety of habitats indicates large differences in response (Table 1). For

example, recovery times ranged from 10 to 70 days in patches b0.2 m2 in size and from 12

to 80 days in patches ~0.4 m2 in size, and there are no clear differences among intertidal

and subtidal habitats. Researchers who have investigated macrofaunal responses to other

types of biogenic structures have also noted varied responses (e.g. Posey, 1986; Dittmann,

1996; Widdicombe et al., 2000). Significant variation can also occur in meiofaunal

responses (e.g. Reidenauer and Thistle, 1981; Sherman et al., 1983, Cross and Curran,

2000). Differences in the effects biogenic patches have on macrofaunal communities are

likely related to patch characteristics and the response of species relative to their life

histories (Zajac and Whitlatch, 1991), and sizes and life styles (e.g. tubiculous or motile),

generating the temporal mosaic nature of soft-sediment systems as argued by Johnson

(1973).

Table 1

Summary of infaunal responses to non-human biogenic disturbance patches across a variety of habitats

Reference Hab Patch

dynamics

Method Recovery rate/

community responses

Van Blaricom,

1982

SS ?, 5% day�1,

~2 weeks

EP, NP,

~0.07 m2,

56 days

14–42 days, SDS, pits

attracted mobile epifauna

Levin, 1984 IM 8–50%,

N1 week

EP, 0.4 m2,

40 days

b40–76+ days, SDS, LHD

Oliver et al.,

1985

SS ?, b80 days EP, 0.07 m2,

80 days

N80 days, dominants lower

in pits, larger worms higher

Oliver and

Slattery, 1985

SS N30%,

2–8 months

EP, NP, 1 m2,

60 days

crustacean exploitation,

others 2–8 months

Thrush, 1986a SS c1%,

c2 weeks

EP, 0.07 m2,

48, 22 days

b48 days, abundances higher

in pits year 1, lower in year 2

Savidge and

Taghon, 1988

IS ? EP, 0.01 m2,

24 days

10–23 days, pits generallyN

ambient, (300 Am)

Hall et al., 1991 SS c3.6%,

1–22 days

EP, 0.20 m2,

24 days

24 days, abundances lower in

pits, particularly larvae.

Natural pits had reductions

but not dominants

Thrush et al.,

1991

IS 5.6–9.8%,

4–7 days

NP, 0.50 m2,

12 days

1–N12 days, bivalves more

rapidly than polychaetes,

no exploitation of pits

Netto and De

Cunha Lana,

1994

IS 50%,

b2 weeks,

EP, 0.008 m2,

18 days

10 days, pit abundances

lower than ambient (250 Am)

This study

(pits only)

IM 10%,

b3 weeks

NP, b0.04 m2,

42 days

21 days, SDS, LHD

Hab=habitat (IM=intertidal mudflat, IS=intertidal sandfalt, SS=subtidal sands). Patch dynamics column provides

estimates of % areal coverage and longevity of pits. Method column indicates whether experimental (EP) or

natural patches (NP) were used, the size of the experimental pit and the duration of observations. Recovery rate

column indicates days to population/community recovery and whether size differences among ambient and

disturbance patches were significant (SDS), and/or colonization modes were life history dependant (LHD). Unless

noted, all studies used a 500-um sieve and only pits were considered. Entries are arranged by year of publication.

R.N. Zajac / J. Exp. Mar. Biol. Ecol. 313 (2004) 297–315 299

Most studies of patches created by feeding activities by epifauna have focused on pits,

using experimental pits to assess differences in abundance among patch types and

recovery patterns (Table 1). This approach stemmed from hypotheses linking dispersal of

adults and juveniles as potential recolonizers of small-scale disturbances (e.g. Eckman,

1983; Gunther, 1992), and the potential of pits to trap organisms and food (Nowell and

Jumars, 1984; Yager et al. 1993) entrained in near-bottom flows. None of the studies

reviewed in Table 1 assessed infaunal responses to mounds that may have been created as

part of the disturbance created by pit digging. However, biogenic mounds created by

subsurface burrowers such as callianassid shrimp have been shown to influence

macrobenthic abundances and distributions (e.g. Posey, 1986). Some researchers have

noted the potential for local variations in response to these disturbances (Thrush, 1986a,b),

but this has not been studied to any great extent. Often, the patch dynamics of pits and

mounds as structural units in benthic landscapes (or benthoscapes) are not quantified. For

example, it is often not known how much of the benthoscape they occupy, how their sizes


change over time, how long they last and at what rate new patches are created.

Concomitantly, these patch characteristics may affect infauna in somewhat less obvious,

but none-the-less ecologically significant ways.

Whilst the effects of biogenic disturbances appear to be variable, they perhaps are not

pathological. That is, there may be cause/effect components that we might be able to

ultimately elucidate, and in doing so account for greater amounts of small-scale variation

in our attempt to understand larger-scale dynamics. Here, I present a study of the dynamics

of pit and mound patches created by crabs on an intertidal mudflat. The objectives of the

study were to (a) quantify the structural dynamics of the patches as components of an

intertidal benthoscape, and (b) assess what effect patch structure and dynamics had on

infaunal populations, both with respect to the specific patch types created by the biogenic

disturbance and the contribution of local community differences. Specific questions

addressed were: (1) Are there differences in infaunal population abundances among pits,

mounds and ambient patches and how do these change over time? (2) How do

recolonization/recovery processes vary among pits and mounds? (3) Do responses differ

among juveniles and adults? (4) To what extent does local variation in pit/mound systems

contribute to population and community responses?

2. Materials and methods

2.1. Study area and pit mound patch characteristics

The study was conducted on a mudflat on the east side of the River Plym estuary in

southwestern England in Plymouth, near Saltram (50823VN; 4806VW) between April and

June 1994. Bait digging occurs in seaward portions of the river and along the west bank

(Cowie et al., 2000). No bait digging was ever observed at the site. Pits and associated

mounds were created by the shore crab, Carcinus maenas either via their feeding

activities, or during burial.

In this study, the biogenic structures created on the tidal flat were considered as pit–

mound (P–M) systems. That is, when crabs dig into the sediments a set of patch types

are created consisting of a pit, a mound of sediment displaced from the pit and the

adjacent ambient sediment that was not dug or covered by mounded sediments. To

assess the dynamics of P–M patches, several sets of data were collected. To determine

whether the number of P–M varied with tidal position, they were counted in 64 adjacent

0.16 m2 quadrats along three transects (~25 m long) located in the lower, middle and

upper intertidal zone. To assess changes in P–M density over time, the number of P–M

were counted in 30 to 45 quadrats in the mid-intertidal approximately every week over a

5-week period. Concurrently, the size of individual P–M systems found along the

transects were estimated. The quadrats were divided into 100 smaller sections (4�4 cm)

and the percent cover of pits and mounds relative to ambient sediments were estimated

by counting the number of blocks occupied by any portion of the mound and pit of the

individual P–M system.

P–M dynamics, i.e. changes in the area of pits and mounds, and pit depth, were

followed over the study period by taking measurements of marked natural P–M systems


and also artificially created P–M systems. On each field date, 10–15 natural, newly created

P–M systems were marked and photographed with a ruler for scale. Newly created pits

were identified by the presence of black sediments both in the pit and on the mound,

indicating recent excavation of reduced, subsurface sediments. Field observations indicate

that these P–M were 0 to 2 days old. In addition to natural pits, a series of 10 artificial P–M

systems were created, marked and photographed. Artificial P–M systems were created by

digging a pit ~3–4 cm deep using a trowel and depositing the sediments on the surface.

Both natural and artificial P–M components were measured in the field. The longest two

axes perpendicular to one another of the pits and mounds were measured as well as the

depth of the pit relative to the local ambient sediment surface. If the pit or mound were

particularly variable in shape several additional width measurements were made. The

marked pits were then re-measured on the following sampling date to track changes in P–

M size. New natural and artificial pits were marked/created on each of the first three

sampling dates. On the third sampling date, 10 additional sets of P–M were marked to

follow longer-term changes to the end of the study period. To minimize trampling of the

study area, set bpathwaysQ were used and all transects and P–M systems sampled were at

least 0.5 seaward of the pathways.

Quadrat data were used to calculate the area of pits and mounds relative to ambient

sediments over the study period. The sizes of pits and mounds based on field data were

calculated by averaging the major axes, taking their mean, dividing by two and then using

this number to calculate the area of a circle. P–M systems that were photographed were

analyzed using Sigma Scan image analysis software. Photographs were scanned and the

digital images were analyzed by tracing the boundaries of the pit and mound in each P–M

and calculating their area. For a number of P–M systems, both field and photograph-based

area estimates were made and comparisons indicated that area calculations based on field

measurements underestimated the actual pit and mound areas. Regression analysis

indicated that field (F) and photographic (P) estimates were related by the equation: P-

area=(2.3314) F-area (n=28, R2=0.7240), which was used to correct all field-based

estimates prior to subsequent analyses.

2.2. Macroinfaunal sampling

Macroinfauna were sampled by randomly selecting three P–M from the set of newly

created P–M identified in the study area, as well as three P–M from the set identified

from the previous sampling date that were 1 week old. On later sampling dates, 2- and

3-week-old P–M systems were sampled similarly. In each system, a core sample was

taken in the middle of the mound and the pit and in a random location in the adjacent

ambient sediment. All cores were identified as coming from specific P–M systems. The

cores were 3 cm in diameter by 5 cm deep. These were capped and returned to the

laboratory where they were transferred to containers and fixed using 4% formalin.

Subsequently the samples were washed on a 212-Am sieve and the residues preserved

in 70% ethanol. Prior to sorting, the samples were washed over nested 500 and 212 Amsieves to separate large and small infauna. For some of the species, this effectively

separated adults and juveniles (see below). Macrofauna were sorted and then identified

to the lowest possible taxon.


2.3. Statistical analyses

Differences in P–M densities, sizes and area coverage among sites and sampling dates

were analyzed using nonparametric Kruskal–Wallis tests. Variance to mean ratios were

calculated to determine P–M dispersion patterns. To determine general differences in the

abundances of individual taxa among pits, mound and ambient sediments over the study

period, data from 0- and 1-week-old pits were combined and analyzed using two-way

analysis of variance (ANOVA), with separate analyses for large and small individuals (i.e.

the 500- and 212-Am size groups). To track changes in the abundance of macrofauna

relative to P–M age and patch type (i.e. pit, mound and ambient), P–M of specific ages

from the last four sampling dates were analyzed using two-way ANOVA. For all univariate

tests, data were tested for normality and homogeneity of variances assumptions, and

transformed (log(x+1)) as needed.

Analyses of macrofaunal responses to P–M dynamics focused on four taxa: three

polychaete species; the spionid Streblospio shrubsolii, the nereid Nereis diversicolor and

the sabellid Manayunkia aestuarina, and several oligochaete species (primarily

Tubificoides benedii and Paranais sp.) which were grouped for the analyses. These taxa

comprised N95% of all the individuals found on the tidal flat. Additional information on

the infaunal community in this portion of the River Plym estuary can be found in Cowie et

al. (2000).

Univariate and multivariate analyses were conducted to determine to what extent local

variation may have been causing differences in macrofaunal responses to the disturbances

and subsequent recovery patterns. One-way ANOVA was used to test differences among

individual P–M systems of specific ages. Only the ambient and mound portion of each P–

M was used in the analyses because large reductions in macrofaunal abundances in the pits

increased variation in overall abundance, masking potential local effects. Non-metric

multidimensional scaling (MDS) was used to assess local differences at the community

level using total abundances found in 0- and 1-week-old P–M systems (mound and

ambient patches only) over the study period. A Bray–Curtis similarity was calculated

using non-transformed data, and the resultant similarities used in the MDS analysis.

Multivariate analyses were performed using PRIMER software (Clarke and Gorley, 2001).

3. Results

3.1. Pit–mound patch dynamics

Large-scale benthoscape structure at the study site was relatively homogenous, being

comprised of large expanses of intertidal mudflat with scattered drainage channels. There

were no other evident large- and meso-scale benthoscape elements, and as such

benthoscape heterogeneity was primarily evident at small spatial scales, and specifically

related to the P–M patches found throughout the mudflat. The number of P–M was not

significantly different among tidal elevations (Kruskal–Wallis test, v24df =3.188,p=0.538), although there was a slight decrease at higher tidal elevations. Temporal

variation in the number of P–M was low over the study period (Fig. 1). The number of

Fig. 1. Variation in the density (F1 standard error (S.E.)) of pit–mound systems in the Plym River intertidal study

site per sampling quadrat and extrapolated to 1 m2. Also shown is the change in the variance to mean ration as a

measure of spatial dispersion.


patches increased slightly after the first week of the study and then remained at ~0.5 P–

M quadrat�1 (or ~3.5 m�2). Temporal changes in the number of P–M quadrat�1 were

marginally significant (Kruskal–Wallis test, v24df =8.49, p=0.075), with the only differ-

ence being between the June 2 and June 9 sampling dates, based on Kruskal–Wallace z-

tests among individual dates. Variance to mean ratios suggest that the P–M were evenly

dispersed across mudflat as most values were b1 (Fig. 1), however these were not

significantly different from random. On June 17, the variance to mean ratio was above

1, and marginally significant ( pc0.10), suggesting a somewhat clumped distribution at

this time. The mean area occupied by the P–M varied from 5% to 10% of the mudflat at

any one time, but ranged to as high as 40% cover in some areas. Temporal changes in

per cent cover were not statistically significant over the study period (Kruskal–Wallis

test, v24df =2.697, p=0.441).Artificial pits steadily decreased in total area over successive sampling dates and

appeared to last ~3 weeks (Fig. 2). In contrast, the total area of natural P–M systems

increased in size after 2 weeks, almost doubling from ~800 to 1400 cm2 and were found to

last b3 weeks. This difference is likely due to the way artificial P–M were created

compared to those naturally formed by crab bioturbation (see Discussion). The increase in

the area of natural pits after 1 week was primarily due to an increase of the mound portion

of the patch, although pit area also increased slightly. Increases in mound area were due to

significant slumping and spreading of the mound when P–M were between 0 and 1 week

old. Increases in pit area were likely due to slumping of the pit walls. Changes in the mean

total area of natural P–M were significant over their lifetime (Kruskal–Wallis test, v22df =

7.707, p=0.021), with total areas at 1 week being significantly larger than at 0 and 2 weeks

(Kruskal–Wallis z-tests among individual P–M ages). The depth of the natural pits

decreased rapidly from ~3 cm when created to several millimeters after 2 weeks.

Fig. 2. Changes in the area of pit and mound patches (top), and depth of pits (bottom) in natural and

experimentally created P–M systems during the study.


The information collected on P–M densities, areal coverage and the dynamics of

individual P–M patches allows for a calculation of the amount of overall sediment

disturbance that occurs on the mudflat due to the creation and eventual erosion of the P–M

patches. Using a value of 10% cover at any one time, and a P–M life span of 2 weeks, then

100% of the mudflat would be disturbed via the creation of P–M patches every 20 weeks.

Assuming that the rate of patch creation and loss is constant over the year, this would

result in the entire mudflat being disturbed 2.6 times every year.

3.2. Macrofaunal responses to P–M dynamics

The spionid Streblospio shrubsolii was the most abundant species during the study

period, reaching densities of ~493,000 individuals m�2. Ambient abundances of

juveniles increased after the first week of the study and did not fluctuate to any great

extent thereafter (Fig. 3). Adult abundances were relatively constant over the study

period but increased by week 5. Abundances in pits were significantly below those

Fig. 3. Fluctuations in mean abundance (F1 standard error) of the numerically dominant taxa in 0- and 1-week-

old P–M systems over the study period. Filled symbols represent small individuals, open symbols represent large

individuals; both size-classes were combined for M. aestuarina. Lines connect means in ambient sediments. Core

size is 3.0 cm diameter.


found in ambient and mound patches for both adults and juveniles (Table 2, Fig. 3).

Although there were no overall statistical differences among ambient and mound

abundances, during the fourth week of the study abundances of adult and juvenile S.

shrubsolii were considerably higher in mounds than in ambient sediments. Oligochaetes

exhibited significant declines in abundance over the study period from ~56,340 to

~14,000 individuals m�2 (Fig. 3) and both large and small individuals were significantly

less abundant in pits. There were no differences in oligochaete abundance among

ambient and mound patches. Adult densities of N. diversicolor did not vary significantly

and remained at ~2800 individuals m�2 over the study period. In contrast, juvenile N.

diversicolor fluctuated considerably, and both juvenile and adult abundances were

significantly lower in pits. The abundance of M. aestuarina generally increased during

the study period from about 21,100 to 109,750 individuals m�2 (Fig. 3). Abundances of

M. aestuarina were significantly lower in pits, and mound and ambient densities did not

differ statistically on an overall basis (Table 2). However, mound abundances tended to

be higher on three of five sampling dates and pit abundances were well below ambient

levels only on two dates (Fig. 3).

Recolonization of P–M systems varied among the four taxa examined, but all sizes

and taxa eventually recovered to ambient levels by 4 weeks (Fig. 4). Over the portion

of the study period that recolonization was examined, juvenile Streblospio shrubsolli

declined and adults increased slightly in ambient sediments. A significant patch type/

age interaction (Table 3) indicates that P–M patches differed significantly from ambient

areas during the first two weeks of recovery. Juvenile abundances in pits were lower

than in ambient sediments at 0 and 2 weeks, and mound abundances were higher at 1

Table 2

Results of statistical analyses (two-way ANOVA) of changes in macrofaunal abundances over time in 0- and 1-

week-old P–M systems

Date Patch type Date/patch interaction

Total abundance 0.0011 b0.0000 0.4350

1b4,5 PbA/M

Streblospio shrubsolii

Juveniles 0.0002 b0.0000 0.6929

1b2,4,5 PbA/M

Adults 0.0088 b0.0000 0.9235

1b5, 3b5 PbA/M

Nereis diversicolor

Juveniles 0.0003 0.0003 0.8779

1b5,2 PbA/M

4b2

Adults 0.9527 0.0030 0.5795

PbA/M

Oligochaetes

Small b0.0000 b0.0000 0.9637

5b4,1,2 PbA/M

3b1,2

Large b0.0000 0.0009 0.257

5,4,3b1,2 PbA/M

Manayunkia aestuarina

All sizes 0.0007 b0.0000 0.5654

1b4,5 PbA/M

Shown are the p values calculated for each factor, and below that, results of Tukey–Kramer multiple-comparison

tests showing dates and patch types that were significantly different ( pb0.05). Dates 1, 2, 3, 4, 5 correspond to the

sequence given in Fig. 3; P=pit, M=mound, A=ambient; degrees of freedom: 4 for Date, 2 for Patch Type.


week. For adult S. shrubsolli, pit abundances were lower at 0 and 1 week, and mound

abundances were higher at 1 week. Adult abundances recovered to ambient levels by 2

weeks and juveniles by 3 weeks. Both adult and juvenile N. diversicolor densities

changed significantly over time, but neither showed differences relative to pit and

mound patch types (Fig. 4, Table 3). However, densities of juveniles in pits were much

lower than ambient levels just after disturbance, and mound abundances were double

ambient levels at 1 week (Fig. 4). Densities of small oligochaetes differed significantly

over time and among patch types. Pit abundances were significantly lower from mound

and ambient sediments on all dates indicating no recovery of these organisms by the

end of the study period. Adult differences were marginally ( pb0.10) significant (Table

3). The significant interaction term indicates variation in response among patch types

over time. Lower abundances of large oligochaetes were found in pits at 0 and 2

weeks relative to ambient levels, but higher abundances at 1 week (Fig. 4). Mound

abundances of large oligochaetes were also higher at this time. Responses of M.

aestuarina were highly variable, particularly in pits (Fig. 4) and, as such, no

significant P–M age or patch type effects were detected during the recolonization study

(Table 3). However, abundances in mounds were higher than in ambient sediments

between 0 and 2 weeks.

Fig. 4. Recolonization patterns (mean abundance F1 standard error) of the numerically dominant taxa in natural

P–M systems relative to the age of the P–M systems. Filled symbols represent small individuals, open symbols

represent large individuals; both size-classes were combined for M. aestuarina. Lines connect means in ambient

sediments. Core size is 3 cm diameter.


Differences among individual P–M systems were tested using only the mound and

ambient data for each P–M system because pit abundances were highly variable and

would have masked any trends in local differences. These analyses indicate that

differences among individual P–M systems varied depending on age of the system, the

taxa considered and their ages/sizes (Table 4). S. shrubsolli exhibited significant

differences only among newly created (0 week old) individuals P–M systems for both

adults and juveniles. N. diversicolor juveniles exhibited differential local responses in P–

M systems of each age, except age 1, (including marginally significant results, pb0.10)

but no differences were found for the adults. Small oligochaetes exhibited significant

differences among both 0- and 3-week-old P–M systems, but large individuals among

only 1-week-old P–M systems. No significant differences were found for M. aestuarina.

To assess how local differences may have changed at the community level over the

study period, a multivariate analysis was done using these four dominant taxa and 0- and

1-week-old P–M systems (Fig. 5). These analyses indicate that differences among local

P–M systems for newly created patches (Age=0) were greatest at the beginning of the

study period (weeks 1 and 2), and that for older pits (Age=1) differences were greater at

weeks 2, 3 and 5.

4. Discussion

The results of this study reveal a rich and complex array of variation in the response of

infaunal to small-scale biogenic disturbances. The sources of this variation include species

Table 3

Results of statistical analyses (two-way ANOVA) of changes in macrofaunal abundance relative to P–M system

and age

Age Patch type Age/patch interaction

Streblospio shrubsolii

Juveniles 0.0011 b0.0000 b0.0000

0b2,1 PbA/M

3b1

Adults 0.0003 0.0051 0.0330

0b1,3,2 PbA/M

Nereis diversicolor

Juveniles 0.0023 0.1417 0.3969

3b2,0,1

Adults 0.0104 0.5030 0.6911

0b3

Oligochaetes

Small 0.0003 b0.0000 0.2459

3b2,0,1 PbA/M

Large 0.0881 0.0938 0.0298

Manayunkia aestuarina

All sizes 0.1147 0.1265 0.4052

Shown are the p values calculated for each factor, and below that, results of Tukey–Kramer multiple-comparison

tests showing ages and patch types that were significantly different ( pb0.05). P–M ages are in weeks; P=pit, M=

mound, A=ambient; degrees of freedom: 3 for Age, 2 for Patch Type.


responses to different patch types (i.e. pits vs. mounds), differences among species and

sizes of individuals, local variation at the level of individual P–M systems and temporal

changes in overall responses relative to recruitment periods.

The P–M systems are a somewhat unique, bcoupledQ patch system in the intertidal

benthoscape, consisting of two distinct co-occurring patch types, the pit and associated

mound. These are extremely dynamic, resulting in a collection of patches of different ages

ranging from newly created, distinct P–M systems to those whose physical characteristics

Table 4

Results of statistical analyses (one-way ANOVA) testing differences among P–M systems of specific ages

Species Age 0 (15) Age 1(15) Age 2 (3) Age 3 (3)

Streblospio shrubsolli

Juveniles 0.0400 0.1688 0.1120 0.6182

Adults 0.0215 0.1522 0.9108 0.3842

Nereis diversicolor

Juveniles 0.0232 0.8630 0.0010 0.0831

Adults 0.3323 0.2172 0.3682 0.9288

Oligochaetes

Small 0.0359 0.3462 0.4090 0.0925

Large 0.1370 0.0112 0.16779 0.3186

Manyunkia aestuarina

All 0.5408 0.5934 0.5000 0.9434

Only the ambient and mound portion of the P–M was used in the analyses because large reductions in

macrofaunal abundances in pits increased variation in overall abundance, thereby masking potential local effects.

Number of P–M systems tested for each age given in parentheses. Shown are the p-values calculated by the test.

Fig. 5. Results of non-metric multidimensional scaling analyses showing differences in community structure

among individual P–M systems of different ages. Top panel shows distances among 0-week-old (newly created)

P–M systems and highlights (enclosed points) systems sampled in weeks 1 and 2 of the study. Bottom panel

shows distances among 1-week-old P–M systems during the study and highlights systems sampled in weeks 2, 3

and 5.


have essentially been dissipated to ambient, non-disturbed sediments by erosion and in-

filling. During that process, the physical characteristics of the patches changed

considerably, including an ~100% increase in size just after they are created (Fig. 2).

The relatively rapid changes in the size of the patches and their short persistence likely

result from the process by which they are created. As crabs dig into the sediments and

create the pit, they break apart the relatively soft, yet cohesive sediments, depositing the

bioturbated sediment in a mound next to the pit. The sediment is then eroded by tidal

action and wind generated water movements, resulting in an increase in the mound area.

Slumping of the sides of the pit resulted in an increase in pit area also. Artificial P–M

systems, which were created by digging a pit using a trowel and depositing the sediments

on the surface, did not exhibit these changing patch attributes, indicating the importance of

the crabs’ feeding behavior on subsequent P–M dynamics. Although individual P–M

systems only lasted about 3 weeks, it is estimated that at any one time there were ~3–4 P–

M systems m�2, ranging from 5% to 40% cover depending on P–M area, and that the

study site was turned over about 2.6 times year�1. These results suggest that the creation

of P–M systems throughout the intertidal represented a dynamic and potentially significant

physical disturbance.


Creation of the P–M systems resulted in pits in which the infauna were disturbed not

only by the physical mixing and removal of the sediment, but also potentially removed

via predation by the crabs. The ejection of sediment out of the pit onto the sediment

surface creating a mound potentially disturbed adjacent infauna via burial and the influx

of infauna which were not eaten and displaced with the sediments. There was no

indication that the creation of P–M systems attracted mobile epifauna such as amphipods

in large numbers, which has been observed in several (Van Blaricom 1982; Oliver and

Slattery, 1985), but not all (e.g. Thrush et al., 1991) studies of biogenic disturbances

which create pits.

The pit portion of P–M systems always had significantly lower abundances of

infauna than mounds and adjacent ambient sediments (Fig. 3, Table 2) for both adults

and juvenile (large and small) individuals. There were no indications of exploitation of

pits, nor increased recolonization via passive transport. In no cases were pit abundances

significantly higher than ambient or mound abundances during the recolonization

process (Fig. 4). That just the opposite was the case for newly created and up to 2-

week-old pits indicates that infauna in the pits were significantly reduced via predation

and/or displacement by the pit digging behavior. Furthermore, conditions in the pit

were not conducive for supporting an opportunistic response following the disturbance,

although the community is dominated by organisms that have been shown to be able to

respond opportunistically to disturbances (e.g. Grassle and Grassle, 1974, Zajac and

Whitlatch, 1982). Recovery of pits to ambient conditions occurred within 3 weeks (Fig.

4), with a steady in-filling of the pits by sediment and gradual increases in abundance

likely due to passive dispersal of adults and juveniles. Recolonization patterns varied

considerably among the taxa analyzed. Although there were significant patch/age

effects for each species, except M. aestuarina, patch type effects were only significant

for adult and juvenile S. shrubsolii and small oligochaetes. Patch type effects were

marginally significant for large oligochaetes and no differences were found for adult

and juvenile nereids. Adult N. diversicolor exhibited no differences in recolonization

among patch types and their mobility may result in local abundances equilibrating

fairly rapidly.

Infaunal abundances in mounds were generally not significantly different from

ambient sediments near the disturbance patch, or, in some cases, were higher than in

ambient sediments (Fig. 3). During recolonization, higher mean abundances in mounds

were found for all four dominant taxa at 1 week (Fig. 4). This suggests that deposition

of disturbed sediments onto the sediment surface, creating the mounds, did not have

negative effects on infauna that were buried. Infauna are resistant to moderate amounts

of burial (e.g. Maurer et al., 1986). Higher densities in the mounds may have been due

to the addition of any infauna that were deposited with the sediments from the pit and/or

increased recolonization of the mounds. Observations in the field suggest that errant

polychaetes, such as N. diversicolor, were very active on the mounds as indicated by

numerous tracks that were often visible on mound surfaces. In addition, it is interesting

to note that M. aestuarina exhibited the most positive mound beffectQ with higher

abundances in mounds on most sampling dates. Flow characteristics over and around

mounds (e.g. Dade et al., 2001) may create beneficial habitat conditions for this small

filter feeding polychaete.


Local spatial differences among the individual P–M systems also appear to have

contributed to the overall levels of variation found in this infaunal community.

Differences among individual P–M systems were temporally variable and also varied

with the age of the systems (Fig. 5). Community structure in newly created P–M

systems was more variable during the first two weeks of the study, whilst in the latter

portion of the study individual P–M systems were more similar . This may have

occurred because of increased recruitment during the latter portion of the study,

particularly by S. shrubsolii and M. aestuarina (Fig. 3). In contrast, older P–M

systems were more variable during the latter portion of the study. This may have been

due to differences in the rate at which the topography of individual P–M systems

reverted back to ambient conditions and local variations in recruitment and other

population processes.

These results provide insights as to the nature of the temporal mosaic characterization

first suggested for soft sediment systems by Johnson (1973), in which benthic habitats are

a collection of patches at different successional stages due to regularly occurring

disturbances to the sea floor from a variety of agents. The disturbances caused by

organisms feeding on infauna (Table 1) result in the formation of patch systems comprised

of several patch types, i.e. pits and mounds, adding to variation in community structure

and population dynamics across benthic habitats. The results of this study show that

disturbance effects and subsequent recovery dynamics in individual P–M systems vary

spatially, likely due to local differences in physical processes and population character-

istics. This further contributes to overall community variation, in addition to that attributed

to individual patch components, i.e. reduced abundances in pits and no differences or

elevated abundances in mounds. Additional variation results from differences in response

by different size-classes (and for some species, potential age-classes) of infauna. Given

these dynamics, are disturbances that form P–M systems important in structuring soft-

sediment communities? The answer to this question is difficult to ascertain. Cowie et al.

(2000) working in the same study area, found that disturbance (raking of the sediment

surface) frequencies of 1 week or more (two to three times a week) caused differences in

community structure relative to undisturbed sediments, but lower frequencies (once every

2 months, once a month, and every 2 weeks) did not. These changes comprised reductions

in the abundances of the same suite of dominant species as reported here (Cowie et al.,

2000). Although the experimental disturbance created by Cowie et al. (2000) was different

from that creating the P–M systems, their results suggest that intertidal communities such

as that studied in the Plym River, are resilient to low levels of disturbance, but that higher

frequencies act to reduce abundances of all the dominant species. Although the rate of new

patch formation was not assessed directly in my study, the estimated turnover of the

sediments in the study area 2.6 times year�1 suggests that the formation of new pits can be

considered a frequent local disturbance. This, and the significant declines in local

abundances of the dominant species in pits, suggests that the creation of P–M systems play

an important role in structuring the intertidal community, particularly in generating

variation across the intertidal landscape and creating the temporal mosaic. This local

variation can have implications for the population dynamics of species in the community,

causing spatial and temporal differences in the population trajectories across the habitat

(Zajac and Whitlatch, 1991). Reversion to ambient conditions occurred by 28 days in the


P–M system, and usually faster in mounds than in pits. This approaches the reproductive

timing of the dominant species at the site, and as such, disturbance patches such as pits

may reduce overall reproductive effort in the population. For example, the densities of

juvenile and adult S. shrubsolii were significantly lower in 1- and 2-week-old pits

throughout the study.

Experimental manipulations of epifauna that generate pits and mounds, and feed on

the infauna, have provided mixed information as to the overall importance of pit–

mound dynamics to community structure. Working in a similar and nearby study site,

Gee et al. (1985) found that crabs, C. maenas, had significant effects on infaunal

populations but that these differed depending on crab size. M. aestuarina and S.

shrubsolii increased in small crab exclosures, whilst abundances were significantly

lower in crab enclosures. Large crabs appeared to cause an increase in the number of

small annelids and this was suggested to be the result of opportunistic responses to

sediment disturbances caused by their burrowing activity (Gee et al., 1985). However,

it does not appear that Gee et al. (1985) sampled pits and mounds specifically. Scherer

and Reise (1981) showed significant declines in infaunal abundance in enclosures with

large (N2 cm carapace width) crabs. Thrush (1986b) found mixed responses using

predator enclosures and exclosures in a deep water site, where only one of three

epifaunal species had a significant impact on the dominant infaunal species via

sediment disturbance and feeding. Hall et al. (1993), showed that exclusion of pit

digging crabs from a subtidal sandy habitat for a period of 1 year did not significantly

alter infaunal community structure, suggesting that the absence of this type of

disturbance has no effect on infaunal communities. Thrush et al. (1994) found that

exclusion of rays caused a significant increase in the abundance of certain infauna at

times when rays were present. The differences we find among these studies may be

due to whether the expectation is a change in community-level properties or

differences are mainly manifest at the population level. For example, a decrease in

disturbance may reduce species richness, as predicted by the intermediate disturbance

hypothesis (Connell, 1978; Huston, 1979; Widdicombe et al., 2000). The experimental

work by Gee et al. (1985) and Cowie et al. (2000) in the Plym and this study, suggest

that this may not be the case for estuarine intertidal habitats with a limited pool of

species that are highly adapted, although along different lines, to maintain populations

under dynamic estuarine and intertidal conditions. Thus, community-level difference

may not be apparent until there are large, frequent and/or relatively severe

disturbances. However at the population level, frequent small-scale disturbances may

contribute to generating spatial and temporal differences in population structure and

dynamics which ultimately lead to different overall trajectories over longer time spans.

What is clear is that disturbances caused by pit digging behaviors lead to significant

amounts of variation in infaunal populations over associated spatial scales and temporal

scales. The result of this study suggest that this variation can be due to the type of

patch created by the disturbance, i.e. a pit or mound, by the size (age) of the infauna,

and also by local differences among individual P–M systems across the intertidal

landscape. These types of small-scale disturbances provide a potentially good model to

explore sources of small-scale variation in soft-sediment systems in order to assess

how this variation may influence larger-scale dynamics.


Acknowledgments

This work was conducted while the author was a visiting scientist at the Plymouth

Marine Laboratory. I would like to express my deepest thanks to Richard Warwick for

providing this opportunity and for the brilliant, multifaceted support that he, John

Davey, Mike Kendall and Steve Widdicombe gave to me and my family during this

time. This work is dedicated to their scientific collegiality and friendship. I also thank

Darryl Allen and Chastity Jock for their assistance in the lab, and Simon Thrush and

an anonymous reviewer for comments and suggestions that helped to improve the

manuscript. As always, thanks to Fran, Julia and Katya. [RW]

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macrofaunal responses to pit–mound patch dynamics in an intertidal mudflat: local versus...

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