Science of the Total Environment 569–570 (2016) 361–372

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Science of the Total Environment

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

Macroinvertebrate community assembly in pools created during

peatland restoration
Lee E. Brown ⁎, Sorain J. Ramchunder, Jeannie M. Beadle, &, Joseph Holden
water@leeds, School of Geography, University of Leeds, Leeds, LS2 9JT, UK

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• We assessed the benefits of peatland

pool restoration for aquatic biodiversity.
• Biomonitoring metrics and community
composition suggested different out-
comes to restoration.
• Null model approaches provided a
clearer suggestion that restoration was
successful.
• Analysis of assembly processes should
be used when planning and evaluating
ecological restorations.

a r t i c l e i n f o a b s t r a c t

Article history: Many degraded ecosystems are subject to restoration attempts, providing new opportunities to unravel the pro-
Received 29 March 2016 cesses of ecological community assembly. Restoration of previously drained northern peatlands, primarily to pro-
Received in revised form 10 June 2016 mote peat and carbon accumulation, has created hundreds of thousands of new open water pools. We assessed
Accepted 20 June 2016
the potential benefits of this wetland restoration for aquatic biodiversity, and how communities reassemble, by
Available online xxxx
comparing pool ecosystems in regions of the UK Pennines on intact (never drained) versus restored (blocked
Editor: D. Barcelo drainage-ditches) peatland. We also evaluated the conceptual idea that comparing reference ecosystems in
terms of their compositional similarity to null assemblages (and thus the relative importance of stochastic versus
Keywords: deterministic assembly) can guide evaluations of restoration success better than analyses of community compo-
Ditch-blocking sition or diversity. Community composition data highlighted some differences in the macroinvertebrate compo-
Drainage sition of restored pools compared to undisturbed peatland pools, which could be used to suggest that alternative
Niche end-points to restoration were influenced by stochastic processes. However, widely used diversity metrics indi-
Pond cated no differences between undisturbed and restored pools. Novel evaluations of restoration using null models
Restoration
confirmed the similarity of deterministic assembly processes from the national species pool across all pools. Sto-
Stochastic
chastic elements were important drivers of between-pool differences at the regional-scale but the scale of these
effects was also similar across most of the pools studied. The amalgamation of assembly theory into ecosystem
restoration monitoring allows us to conclude with more certainty that restoration has been successful from an
ecological perspective in these systems. Evaluation of these UK findings compared to those from peatlands across

⁎ Corresponding author.
E-mail address: [email protected] (L.E. Brown).

http://dx.doi.org/10.1016/j.scitotenv.2016.06.169
0048-9697/© 2016 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
362 L.E. Brown et al. / Science of the Total Environment 569–570 (2016) 361–372

Europe and North America further suggests that restoring peatland pools delivers significant benefits for aquatic
fauna by providing extensive new habitat that is largely equivalent to natural pools. More generally, we suggest
that assembly theory could provide new benchmarks for planning and evaluating ecological restoration success.
© 2016 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license
(http://creativecommons.org/licenses/by/4.0/).

1. Introduction contrast, if stochastic dispersal events or internal dynamics are impor-

tant drivers of assembly (Belyea and Lancaster, 1999; Heino, 2012),
Degraded, damaged or destroyed ecosystems are the subject of ever communities in restored wetland sites might not fully resemble those
increasing attempts to effect restoration of ecological processes, conserve in reference sites even if environmental conditions show no difference.
biodiversity and sustain the livelihoods of people who depend upon them Peatlands cover ~4 M km2 of northern temperate and boreal regions
(Allison, 2012). Billions of dollars are spent annually on ecosystem resto- (Yu, 2012) and large expanses of N. Europe, N. America and Russia have
ration (Goldstein et al., 2008; Birch et al., 2010), with estimates for the U.S. been impacted by land drainage (Holden et al., 2004; Mazerolle et al.,
alone running to $9.5B per annum (BenDor et al., 2015). Restoration ef- 2006; Hannigan et al., 2011; Beadle et al., 2015). Recognition of the
forts can include the removal of barriers to recovery, reconfiguration of global environmental implications of peatland degradation has led to
habitats, or assistance with species recolonization. Biodiversity increases attempts to rewet drained peatlands, with the aim of restoring the
are often cited as a key goal of restoration (Kirkman et al., 2013). Howev- growth of peat-forming vegetation, promoting peat accumulation and
er, only 35–44% of restoration programmes across a wide range of ecosys- thus enhancing terrestrial carbon sinks (Poulin et al., 2004;
tem types have been reported as having favourable outcomes for Ramchunder et al., 2009). UK blanket peatlands (Fig. 1) have historically
biodiversity (Benayas et al., 2009; Jones and Schmitz, 2009) leading to been subjected to intensive drainage to lower the water table in at-
the often repeated conclusion that many ecological restoration attempts tempts to make the land more suitable for agriculture, gun-sports, com-
have been unsuccessful (Lockwood and Pimm, 1999). mercial forestry or for peat extraction for use as fuel or in horticulture
A typical focus of ecosystem restoration monitoring is the assess- (Holden et al., 2007). Large-scale restoration practices have created
ment of empirically measurable attributes of a community such as di- hundreds of thousands of open water pools, ponds and lakes (Beadle
versity and abundance (Seabloom and Valk, 2003; Klimkowska et al., et al., 2015) but to date they have received relatively little attention
2007; Palmer et al., 2010), biomonitoring index scores (Bonada et al., with respect to their biodiversity and/or community (re-) assembly
2006), indicator species abundance (Pykälä, 2003; González et al., compared with studies of their hydrology, chemistry and gas emissions
2013) or aspects of ecosystem functioning (Lepori et al., 2005; Foster (Haapalehto et al., 2011). Despite the potential importance of new bog
et al., 2007) relative to control or reference sites. A potential reason pools for aquatic biodiversity, these habitat features are also potential
for the reported low success rates, and often unexpected results of eco- hotspots for the release of both CH4 and CO2 (Cliché-Trudeau et al.,
logical restoration, is that structural and functional attributes of ecosys- 2012). This is important because some consideration is being given to
tems can reach alternative states as post-restoration succession infilling ditches, rather than creating pools, to reduce greenhouse gas
proceeds (Suding et al., 2004; Hobbs, 2007). Significant drivers of releases (Parry et al., 2014). It is therefore vital that the biodiversity of
changes in ecosystem structure and functioning include dispersal and these habitats is studied to provide a balanced research base that can in-
colonisation success, biotic interactions and feedbacks which can intro- form future management and conservation decisions.
duce significant stochasticity to community composition (Ledger et al., This study investigated the physicochemical characteristics and mac-
2006; Chase, 2007; Heino et al., 2015) and thus to restoration outcomes. roinvertebrate communities of natural versus artificial pools ecosystems,
However, incorporating knowledge of reference-community assembly with the aim of first providing a comparative evaluation of their macroin-
processes in the planning or evaluation of restoration programmes has vertebrate community composition. Specifically, we sought to answer the
still not begun (Lockwood and Pimm, 1999; Chase, 2007). question: do restored pool environments support assemblages similar to
Where environmental conditions do not impose excessively strong naturally formed pools? Second, the integration of ecological theory with
controls on biodiversity, there is often a distribution of potential restora- practice has been a long-standing goal of restoration (Temperton et al.,
tion end points which arises rather than a single definable end point 2004; Hobbs, 2007), and here we evaluate the benefits of such an ap-
(Chase, 2007; Milner et al., 2011). In conceptual terms, evaluating restora- proach to assess restoration success alongside widely used measures of
tion success based on a system's ability to assemble towards this range of community composition and diversity metrics. Third, we evaluated
states should be desired by practitioners where it is also the case in their whether or not these pool systems contain biota similar to pools on re-
reference system(s). However, a general focus by restoration practitioners stored peatlands elsewhere in the northern hemisphere, to shed light
on restoring abiotic habitat to deliver quite specific biodiversity outcomes on the potential to generalise our findings of deterministic versus stochas-
means that deterministic (niche) processes of community assembly tic constraints on peatland pool macroinvertebrate communities.
(Belyea and Lancaster, 1999) are essentially a major consideration within
restoration design. In these cases, restoration is only likely to be deemed 2. Methods
completely successful where it is aimed at ecosystems that already have
strong deterministic assembly processes which serve to ‘filter’ (Poff, 2.1. Study sites
1997; Fattorini and Halle, 2004) the species pool towards a narrowly de-
fined end point, similar to the reference state. The study examined 40 independent bog pools (20 natural, 20 arti-
In environments such as wetlands, which have been degraded his- ficial) on three occasions in the Pennines of northern England, UK. Po-
torically via land drainage activities, heterogeneity may be decreased tential sites with pools were identified using aerial images available
following rewetting which aims to homogenise water-table variations online. All shortlisted sites were visited to ground-truth the manage-
and vegetation across a site (Verberk et al., 2010). In such ecosystems, ment techniques and pool size. The final selection of study sites was de-
restoration activities provide ideal opportunities to evaluate biological termined by selecting restored sites with similar lengths of time for
community assembly processes because environmental homogeneity colonisation since peatland restoration had occurred (5–10 years), and
should promote high similarity between the biota of restored environ- where restored peatlands could be compared to nearby intact peatlands
ments and local reference sites, especially if environmental conditions with no history of artificial drainage management. Of the 40 pools se-
are harsh enough to serve as deterministic influences on community as- lected for study, 20 were located in the North Pennines region and 20
sembly (Thompson and Townsend, 2006; Brown and Milner, 2012). In in the South Pennines (10 pools on undisturbed peatland vs 10 pools
 L.E. Brown et al. / Science of the Total Environment 569–570 (2016) 361–372 363

Fig. 1. Photographs of pools located on blanket peatland in the UK uplands: (a) and (b) series of pools created artificially during peatland restoration by the blocking of a drain which runs
away from the foreground, (c) and (d) naturally formed pools (width ~1.5 m to 2 m), (e) map of study locations in the North and South Pennines regions of the UK.

on restored peatland in each region). Pools were all typically up to 2– North Pennines are relatively remote from large urban areas
3 m2 surface area (Fig. 1). The South Pennines region experienced (Caporn and Bridget, 2008); therefore, the study design also allowed
historically higher levels of airborne pollutant deposition from the us to incorporate a consideration of any legacy effects on pool eco-
nearby urban centres of Sheffield and Manchester, whereas the system assembly.
364 L.E. Brown et al. / Science of the Total Environment 569–570 (2016) 361–372

In the north, pools were located within the North Pennines AONB in- 2013). DOC was measured with a Thermalox 8000 total carbon analyser
cluding parts of Upper Teesdale and Geltsdale. Artificially-created peatland (Metrohm UK, Ltd., Buckingham, UK), NO3 with a Dionex 4000i chro-
pools on restored peatland were located at Herdship Fell (54°41′N, 2°21′ matograph in conjunction with an automatic sampler, and Al and Fe
W) and Middle Top Fell (54°53′N, 2°36′W). Naturally-formed pools using an Optima 5300DV instrument (PerkinElmer, Massachusetts, US).
were located across Moor House National Nature Reserve (54°41′N, 2° Macroinvertebrates were selected as a ‘model’ biological group to
23′W). In the South Pennines, study pools were located in the Dark Peak evaluate restoration success because they are ubiquitous in aquatic en-
area. Here artificially-formed pools formed at Winscar (53°30′N, 1°47′ vironments, easy to collect and identify, they exhibit a range of re-
W) were contrasted with naturally-formed pools on Midhope Moor (53° sponses to differences in environmental conditions, and dispersal
28′N, 1°43′W). There were no naturally-formed pools available to sample ability varies between groups. Macroinvertebrate samples were collect-
on the restored peatlands owing to previous drainage activities, therefore ed using a long handled net (250 μm mesh). A total of three minute
the study was designed to make comparisons with the nearest available sampling was undertaken, with 2 min of sampling time divided equally
peatlands that housed natural pools. Artificial pools were selected ran- between observed mesohabitats (i.e. open water, vegetation, pool bot-
domly across the restored peatlands and we avoided sampling pools locat- tom) and an additional 1 min spent searching for pleustonic animals
ed on the same former drainage channels to prevent non-independence of (Nicolet et al., 2004). Samples were preserved in 70% methylated spirits
pool physicochemical and biotic observations. No pre-restoration sam- then, after sorting in the laboratory, macroinvertebrates were identified
pling was undertaken because there were no pools on the drained to species level (where possible) under a light microscope (up to ×40
peatlands prior to drain-blocking. Pools were sampled in Sept. 2011, magnification) using standard keys (Pawley et al., 2011 and references
March 2012 and June 2012. Sampling was also planned during Dec. therein). Whilst identification at mixed levels of taxonomy might have
2011 but was not possible as all of the pools were frozen at the surface. modified the summary metrics and community analyses we generated,
All sites had blanket peat cover, with vegetation dominated by there was necessarily a trade-off between identifying the most abun-
Eriophorum spp. and Calluna vulgaris (L.). There was Sphagnum spp. dant groups such as Chironomidae to species level to maximise the abil-
cover at all sites, but this was less abundant in the South Pennines. Con- ity to discriminate between samples (Jones, 2008), versus coarser
textual meteorological data were not available for all sites but, for exam- identification of less common taxa for which larval identification be-
ple, mean annual precipitation of 2012 mm (1951–1980; 1991–2006) yond Family is difficult (e.g. other Diptera). Chironomidae were sub-
occurs at Moor House (Holden and Rose, 2011) and 1123 mm (1961– sampled (n = 50) where abundance per sample was N50 individuals.
1990) at Geltsdale reserve, North Pennines (Jonczyk et al., 2009), and Individuals were cleared in 10% KOH, transferred to 99.85% glacial acetic
from 1000 to 1584 mm across the South Pennines (Evans and Jenkins, acid for 5 min, rinsed in ethanol and then mounted on slides using
2000). Mean annual air temperature at Moor House is 5.3 °C (1931– Euparal. Chironomidae were identified using Rieradevall and Brooks
2006 (Holden and Rose, 2011)) and in the South Pennines mean month- (2001) and Brooks et al. (2007).
ly temperatures range from 2 to 14 °C (Evans and Jenkins, 2000).
2.3. Data analysis
2.2. Field sampling
Non-metric multidimensional scaling (NMDS) was used to investi-
At each pool on each sampling date, nine environmental variables gate how community composition (based on square-root transformed
were measured to contrast physicochemical habitat between pool abundance data) varied between region, pool type and between sam-
types. Measurements of physicochemical variables that are key influ- pling dates, using the Vegan package (Oksanen, 2005) in R. Bray-Curtis
ences on aquatic macroinvertebrates focused on water temperature, dissimilarities were used and the best two-dimensional solution
pH, dissolved oxygen (DO) and turbidity. A Hach Lange (Salford, UK) retained following up to 200 restarts. Physicochemical variable vectors
HQ30d handheld probe was used for the first three measurements, were fitted to the solution post-hoc using the envfit procedure with
and turbidity was measured using a Hanna Instruments 93,703 turbid- 999 permutations. This approach was preferred over direct ordination
ity meter. At each pool, average depth was calculated from seven ran- approaches such as RDA/CCA because NMDS makes no assumptions
dom measurements. Additionally, 50 mL of water was passed through about the underlying data structure, and better represents the distances
a 0.45 μm filter and subsequently analysed for key nutrients (NO3, dis- between samples in ordination space (Legendre and Legendre, 1998).
solved organic carbon (DOC)) and metals (inorganic Al, Fe) that can in- PERMANOVA was undertaken using the Vegan package (Oksanen,
fluence the abundance of some sensitive invertebrate taxa (Brown et al., 2005) in R2.14.0 (R Development Core Team, 2014) to determine

Table 1
Descriptive statistics and GLMM results for undisturbed and restored peatland pool physicochemical variables.

NO3 (mg L−1) Al (mg L−1) Fe DOC DO (mg L−1) pH Water temperature (°C) Turbidity (NTU) Depth (m)
(mg L−1) (mg L−1)

Undisturbed
Mean 0.37 0.13 0.81 39.5 7.84 4.18 13.3 25.8 0.07
Median 0.09 0.07 0.56 28.9 8.82 4.17 14.1 1.9 0.13
Min 0.01 b 0.01 0.05 10.7 0.31 3.80 4.4 0.5 0.02
Max 2.87 0.51 4.35 140.2 15.5 4.70 20.5 750 0.16

Restored
Mean 0.39 0.10 0.66 34.4 8.07 4.07 11.6 2.6 0.15
Median 0.10 0.08 0.60 35.0 8.55 4.08 12.4 1.4 0.07
Min 0.02 b 0.01 0.23 13.4 0.40 3.70 5.3 0.3 0.04
Max 5.31 0.37 1.83 59.3 17.3 4.70 18.2 34 0.37

GLMM results
Region t = −1.52 t = −3.42 t = −1.32 t = −1.48 t = 0.42 t = 2.99 t = −0.52 t = −1.24 t = 0.65
P = 0.23 P = 0.04 P = 0.28 P = 0.23 P = 0.70 P = 0.06 P = 0.64 P = 0.30 P = 0.56
Region:Pool type t = 1.39 t = 0.68 t = −0.68 t = −0.73 t = 1.50 t = 0.60 t = 0.26 t = −0.57 t = −1.40
P = 0.26 P = 0.55 P = 0.55 P = 0.52 P = 0.23 P = 0.59 P = 0.81 P = 0.61 P = 0.26
Region:Pool type:Sampling date t = −1.27 t = −0.90 t = −0.46 t = 0.50 t = −1.61 t = 1.06 t = 0.33 t = 1.05 t = −0.06
P = 0.23 P = 0.39 P = 0.66 P = 0.62 P = 0.13 P = 0.31 P = 0.75 P = 0.32 P = 0.95
 L.E. Brown et al. / Science of the Total Environment 569–570 (2016) 361–372 365

whether there were significant differences in pool macroinvertebrate- in the lme4 package in R (Bates et al., 2015) to determine whether there
community composition between region, pool type and sampling dates. were significant differences in macroinvertebrate community metrics
Macroinvertebrate community structure was summarised for each and pool physicochemical variables as a function of region (North or
sample using the following measures: (i) log10 (total abundance +1); South Pennines), pool type (natural or restored; nested within region)
(ii) taxonomic richness; (iii) 1/Simpson's diversity index (1/S); (iv) tax- and sampling date (three seasons; nested within pool type), with
onomic dominance (D) estimated as D = Nmax/N, where Nmax is the study sites and sampling date included as random factors.
number of individuals in the most abundant species and N is the total To assess the assembly processes of macroinvertebrate communi-
abundance. Additionally, relative abundances (%) were calculated for ties, Jaccard's coefficient of similarity (J) was calculated for peatland
macroinvertebrate indicator groups that are most commonly found in pool samples collected in Sept. 2011, which was the first sampling occa-
peatland pools (Mazerolle et al., 2006; Hannigan et al., 2011; Beadle et sion for each pool. J values were compared against those derived from
al., 2015): Chironomidae, Hemiptera, Coleoptera and Odonata. Beta-di- 1000 null model simulations (Chase, 2007) for national (UK) and re-
versity was estimated using the Bray-Curtis index calculated across the gional (Pennine study sites) species pools. The species pool used to con-
replicate pool samples for undisturbed and restored, separately, on each struct national null assemblages was composed of the 64 taxa identified
sampling date. Mixed-effects general linear models (GLMM) were used from our blanket peatland samples, plus an additional 159

Fig. 2. (a) Site and physicochemical variables (region denoted as NP = North Pennines, SP = South Pennines) - only significant variables (P b 0.05) are shown [dissolved organic carbon
(DOC) R2 = 0.20, P = 0.001; pH R2 = 0.08, P = 0.01; Dissolved Oxygen (DO) R2 = 0.06, P = 0.034; Al R2 = 0.27 P = 0.001; Fe R2 = 0.12, P = 0.002; (b) sites categorised by region and pool
type (A = Artificial, N = Natural); (c) as per panel b for Sept. 2011; (d) as per panel b for March 2012; (e) as per panel b for June 2012; (f) species biplot. Non-metric fit R2 was 0.94, linear
fit R2 was 0.71, and stress was 0.18.
366 L.E. Brown et al. / Science of the Total Environment 569–570 (2016) 361–372

macroinvertebrate taxa that have been reported from open water ponds 1497 inds.) and Hemiptera (11 taxa; 318 inds.). Trichoptera were found
throughout the UK (Pond Action, 1991; Nicolet, 2001; Nicolet et al., in low abundance but included Limnephilus coenosus which is common
2004; Hill and Wood, 2014). The peatland taxon pool that this analysis fo- in small permanent peatland pools, as well as Polycentropodidae
cused on is a subset of the national taxon pool. The peatlands that were (Polycentropus sp., Plectrocnemia conspersa and Holocentropus spp.).
restored had no ponds previously due to land drainage activities, and Small but significant differences in macroinvertebrate community com-
the restoration aimed to create ecosystems that are as similar as possible position were found between pool types (PERMANOVA; R2 = 0.09; P =
to those of the undisturbed, intact peatlands. Therefore, our aim with this 0.001), region (R2 = 0.17, P = 0.001) and pool type*region (R2 = 0.09;
analysis was to assess whether the communities that assembled from the P = 0.001) despite pool environments showing no significant differ-
national taxon pool in the restored site pools were similar to those on in- ences in physicochemistry between pool types, either when combined
tact peatlands, which have also assembled from the same national taxon overall or when nested within sampling dates (Table 1).
pool. The national taxon pool was used because immigration into restored Samples collected in Sept. 2011 were most dissimilar, plotting in the
peatlands would not be restricted exclusively to taxa found only on our positive regions of NMDS axis 1 compared with samples collected in
study peatlands. However, if the restoration was successful then success- 2012 (Fig. 2). Axis 1 of the NMDS was associated with shifts in compo-
ful establishment of immigrants will mirror the intact peatland taxon pool. sition from Corynoneura scutella, Limnephilus coenosus, Polypedilum
For comparative purposes, we created regional null models using only the nubifer, Polypedilum nuberculosum and Helophorus brevipalpis (negative
64 taxa found within our Pennine sampling pools. As these assemblages region) to communities with more Derotanypus, Nemouridae,
were already expected to be ‘filtered’ deterministically from the national Corixidae, Chironomus plumosus and Tanytarsus numerosus (positive re-
species pool due to the peatland location, we expected to see a greater im- gion). Negative regions of axis 2 were associated strongly with
portance of stochastic assembly processes in this analysis reflecting be- Pyrrhosoma nymphula, and small Hydroporus, Orthocladiinae, Dytiscidae
tween-pool differences. A key reason for evaluating restoration success and Limnephilidae that could not be identified to genus or lower. Posi-
using models across both scales was to identify whether the assembly tive regions of axis 2 were associated with higher abundance of
processes were similar between pool types, regardless of the scale used Hydroporus pubescens, Hydroporus obscurus, Apsectrotanypus
to underpin the null models. trifascipennis and Psectrocladius (Allopsectrocladius) obvious (Fig. 2).
Null models were controlled for the taxonomic richness of each sam- Several physicochemical variables fitted significantly to the NMDS
ple by randomly permuting the presence-absence of taxa within samples, using ordifit, with higher pH and dissolved oxygen concentration asso-
using the permatfull procedure in Vegan. If community assembly was ciated with the samples collected in 2012.
dominated by stochastic processes of dispersal/priority effects then ob-
served and expected values would show no significant difference (i.e. 3.2. Community diversity metrics
mean observed values similar to mean null predictions) (Chase, 2007).
Null modelling approaches based on taxonomic identity (Chase, 2007) In contrast to the community composition findings, no differences
were preferred over those based on biological traits (Brown and Milner, were observed between region, pool type or sampling date for the mac-
2012) because of the overwhelming dominance of Chironomidae, for roinvertebrate metrics that we calculated (Table 2; Fig. 3). Chirono-
which traits are defined poorly below subfamily level. To determine effect midae were typically the dominant indicator group and abundances
sizes, null model estimates were subtracted from observed J values then were similar for both pool types at N80% on average (Fig. 4), numbering
compared between pool types x region using GLM. 100% in some pools (Table 2). No significant differences were found for
Coleoptera, Hemiptera and Odonata relative abundance (Table 2, Fig. 4).
3. Results
3.3. Community assembly processes
3.1. Macroinvertebrate community composition
Analysis of all pool samples combined revealed a mean beta-diversi-
From 120 individual pool samples, 28,217 individual macroinverte- ty (Jaccard's co-efficient of similarity [J]) of 0.34 (95% Confidence Inter-
brates were identified across 64 taxa. Most taxa belonged to the Chiron- vals = 0.11–0.57) which contrasted markedly with predictions from
omidae (28 taxa; 24,464 inds.), Coleoptera (11 adult taxa, 4 larval taxa; 1000 null model assemblages (national scale mean J = 0.05; 95%

Table 2
Descriptive statistics and GLMM results for undisturbed and restored peatland pool macroinvertebrate community metrics.

Total Richness Simpson's Diversity Dominance Beta % % % %

abundance (1/S) (D) diversity Chironomidae Hemiptera Coleoptera Odonata

Undisturbed
Mean 226 5 1.6 84.5 0.31 82 1 11 0
Median 225 5 1.2 91.7 0.31 91.7 0 3 0
Min. 7 2 1.0 33.3 0 14 0 0 0
Max. 742 10 6.1 99.0 0.85 99 7 81 0

Restored
Mean 244 8 1.6 80.4 0.33 80 2 9 0
Median 220 8 1.3 86.3 0.31 86.3 0 5 0
Min. 30 1 1 41.7 0.04 27 0 0 0
Max. 737 15 4.7 100.0 0.79 100 13 57 11

GLMM results
Region t = −0.41 t = 1.90 t = 0.88 t = −1.07 t = 1.83 t = −0.84 t = 1.00 t = 0.39 t = 1.13
P = 0.71 P = 0.15 P = 0.45 P = 0.36 P = 0.14 P = 0.46 P = 0.39 P = 0.72 P = 0.34
Region:Pool type t = 0.88 t= t = 0.67 t = 0.13 t = −1.13 t = 0.21 t = 0.72 t = 0.22 t=
P = 0.44 −0.86 P = 0.55 P = 0.91 P = 0.29 P = 0.84 P = 0.52 P = 0.84 −0.59
P = 0.45 P = 0.60
Region:Pool type:Sampling t = −1.97 t= t = −0.51 t = −0.32 t = 0.42 t = −1.13 t = −1.39 t = 1.42 t = 0.00
date P = 0.07 −0.65 P = 0.62 P = 0.76 P = 0.68 P = 0.28 P = 0.19 P = 0.18 P = 1.00
P = 0.53
 L.E. Brown et al. / Science of the Total Environment 569–570 (2016) 361–372 367

pools indicating they were not significantly different. Effect-sizes be-

tween null expectations and observed values differed between regions
(ANOVA F1,3997 = 21.182, P b 0.001) and pool type within regions
(ANOVA F1,3997 = 51.739, P b 0.001).

4. Discussion

4.1. Community composition and diversity

This study has provided detailed new insights into the biodiversity
and community assembly processes of pool ecosystems on intact and
restored blanket peatland. The dominance of Chironomidae in all
pools was in agreement with findings from other bog pool studies
(Beadle et al., 2015; Table 3). Three sub-families, Orthocladiinae,
Chironominae and Tanypodinae, accounted for the majority of all the
dipterans, similar to Hannigan et al's. (2011) study of peatland pools,
and there was no significant difference in their abundance between
pool types. The relatively low abundance of large invertebrate preda-
tors, the availability of refuge areas (e.g. among abundant moss layers)
and/or mass-effects potentially contribute to the dominance of Chiron-
omidae but experimental manipulations would be required to unpick
these causes. Another reason for the dominance of Chironomidae may
be their ability to adapt their diet to available food sources. All chirono-
mid taxa, even tanypods which are generally classed as predators, will
consume detritus (Baker and McLachlan, 1979) which is abundant in
peatland pools. Some chironomids also eat methanotrophic bacteria
(Jones et al., 2008), and Ruse (2002) noted that many predatory chiron-
omids are also algal-feeders during their early instars. This omnivory al-
lows them to inhabit even the smallest of bog pools, such as puddles on
Kielder Moor, northern England (Jackson and McLachlan, 1991).
Studies in mainland European and North American peatland pools
have suggested that groups such as Coleoptera (Table 3) can sometimes
dominate invertebrate communities, and they were typically the second
most abundant group of macroinvertebrates found in our UK peatland
pools. However, there were no significant differences in relative abun-
dance between natural and artificial pools, most likely reflecting the
similarity in pool physicochemical conditions. Adult Coleoptera have
excellent flight capabilities (Mazerolle et al., 2006) and they readily col-
onise new peatland pool habitats (Table 3). Van Duinen et al. (2007)
suggested that to evaluate the success of bog restoration for aquatic
macroinvertebrates, it is important to examine the colonisation success
of later colonisers such as caddis flies. In our study we observed
Limnephilus coenosus, which is common in small permanent peatland
pools (Wilkinson, 1984). Other caddis observed were
Polycentropodidae (Polycentropus sp., Plectrocnemia conspersa and
Holocentropus spp.). Polycentropus were found on only one occasion in
Fig. 3. Box plots of (a) Total abundance; (b) Richness; (c) 1/Simpson's Diversity; (d) an artificial pool at Middle Top Fell, and Plectronemia were found only
Dominance and; (e) Beta diversity for pools on restored and undisturbed peatland. in artificially formed pools at Winscar and Middle Top Fell.
Holocentropus were found in both pool types but only in Sept. 2011.
The presence of these caddis indicates that these pools are being
CI = 0.04–0.06). For the national-scale null models, null model expecta- colonised successfully by ‘later colonisers’ albeit in low abundance.
tions were similarly low compared with within pool-type J (Undis- Odonata are represented widely in peat pools often being found in
turbed J = 0.39 (95% CI = 0.17–0.61); null mean J = 0.04; 95% CI = large permanent waterbodies (Standen, 1999; Mazerolle et al., 2006)
0.03–0.05; Restored J = 0.42 (95% CI = 0.20–0.64); null mean J = perhaps reflecting the increased availability of prey or oviposition
0.06; 95% CI = 0.05–0.07; Fig. 5a, b), with similar disparities between sites, as well as a need for permanent water coverage for the developing,
observed and null expectations evident when data were split by region. often semivoltine, larvae. In this study, we found only one Odonata spe-
Effect-sizes between null expectations and observed values did differ cies, the damselfly Pyrrhosoma nymphula, at only one artificial pool site
slightly between regions (ANOVA F1,3997 = 1662, P b 0.00001) and (Crook Burn), which is a low number of Odonata species compared to
pool type within regions (ANOVA F1,3997 = 2798, P b 0.00001). reports from restored peatlands in Finland where several species
For the regional-scale null models, within pool-type model expecta- colonised pools within three years (Elo et al., 2015). All other studies
tions were also low (All data combined: mean J = 0.182; 95% CI = of restored peatland have highlighted that new waterbodies are
0.175–0.189; Undisturbed null mean J = 0.15; 95% CI = 0.13–0.16; Re- colonised by Odonata (Table 3), and as further studies of the many thou-
stored null mean J = 0.22; 95% CI = 0.21–0.24; Fig. 5c, d) compared sands of new UK peatland pool habitats are conducted, more records of
with observed J values (as per national analysis above), but overlapped Odonata should become available to better evaluate the provision of
marginally with the lower 95% confidence intervals for the restored habitat for this group.
368 L.E. Brown et al. / Science of the Total Environment 569–570 (2016) 361–372

Fig. 4. Average relative abundance of selected macroinvertebrates groups from (a) all pool samples combined, and across the three sampling dates for (b) pools on restored peatland and
(c) pools on undisturbed peatland.

4.2. Community assembly and/or comparing community diversity indices, produced conclusions
about the effectiveness of peatland restoration that could initially be
Our study provides a new perspective on the utility of incorporating deemed as being in opposition. For example, when evaluating differ-
null modelling approaches to evaluate the outcomes of ecosystem res- ences between undisturbed and restored peatlands using community
toration, illustrating how conclusions about the success or otherwise diversity metrics, our findings of high similarity mirrored other
in terms of biodiversity responses can be contingent upon the approach peatland restoration studies (Hannigan et al., 2011) and suggested
taken to evaluate ecological community properties. The two commonly that the homogeneity of relatively harsh (i.e. low pH, low nutrient status
used approaches of analysing community compositional differences (Hannigan et al., 2011; Turner et al., 2016)) pool environmental
 L.E. Brown et al. / Science of the Total Environment 569–570 (2016) 361–372 369

Fig. 5. Pool type x region boxplots for (a) Jaccard similarity scores for observed – null model predictions (regional null model); (b) null predictions only (regional null model); (c) Jaccard
similarity scores for observed – null model predictions (local null model), and; (d) null predictions only (local null model).

conditions serves as a deterministic influence on community assembly The marked contrast between national-scale null model expecta-
(Verberk et al., 2010). In contrast though, significant (i.e. P b 0.05) tions and observed community similarity values for pool macroinverte-
PERMANOVA results for pool type and region*pool type could be seen brate communities, on both undisturbed and restored peatlands,
to imply that restored pools do not fully resemble the naturally formed confirmed the strong deterministic effect of peatland pool environment
pools in terms of their taxonomic composition, with restoration leading on community similarity (Chase, 2007). Effect-size estimates again sug-
to different end points (Hobbs and Norton, 1996; Suding et al., 2004) gested only minor differences in the strength of deterministic niche fil-
despite the high similarity of pool environments. However, it is impor- ters between the two regions and pool types compared with the overall
tant to note that the effect size of pool type in these analyses was rela- magnitude of the observed vs. null effect-size. The regional null model
tively small (R2 = 0.09); thus, the community composition of natural analysis highlighted detectable differences in the importance of sto-
and restored pools was actually extremely similar for the most part. chastic dispersal assembly processes although, notably, three of the
The minor differences could be attributable to random events of dis- four region/pool type combinations showed similar levels of
persal (Heino, 2012), and/or the establishment sequence of pool stochasticity, offering further evidence of restoration success. Whilst
colonisers, for example via priority effects and biotic interactions with the South Pennines restored pools were similar to those in the North
existing predators, prey and competitors (Belyea and Lancaster, 1999; Pennines, the South Pennines natural pools nevertheless showed more
Ledger et al., 2006). evidence of deterministic effects in the regional null model analysis
Together, our findings from pool physicochemical habitat, biomoni- compared with other locations. This might relate to a legacy effect
toring metrics and community composition point towards these sys- from historic atmospheric pollution sources in this area (Evans and
tems displaying an overwhelming deterministic nature, especially Jenkins, 2000) but more detailed chemistry data are needed to test
from the national species pool. The assembly models provided some ev- this hypothesis. Overall, these analyses suggest that the incorporation
idence for a stochastic element within the regional species pool, al- of assembly process comparisons can potentially provide an additional
though it was similar across the majority of pool locations and types, useful benchmark for evaluating restoration success, than the measure-
driving minor changes in community composition between pool ment of community composition or biodiversity metrics alone.
types. Mixed assembly processes, such as those we have observed in Our novel approach to the evaluation of restoration schemes centres
these peatland pools, are increasingly recognised across a range of eco- on the re-establishment of fundamental assembly processes relative to
systems (Thompson and Townsend, 2006; Brown and Milner, 2012; the reference state. Further work will clearly be needed to test this
Vellend et al., 2014). However, to make robust conclusions about eco- idea in other types of restored habitats. However, by adopting this con-
system restoration success requires an ability to determine more con- cept more widely it should be possible to determine whether alterna-
clusively if these underlying fundamental processes vary or not tive end points of restoration (Suding et al., 2004) are a consequence
between restored and reference conditions. of inadequate restoration approaches in which the assembly processes
370 L.E. Brown et al. / Science of the Total Environment 569–570 (2016) 361–372

Table 3
A comparison of the key findings and conclusions from our study of UK blanket peatland aquatic ecosystems relative to published studies from other parts of Northern Europe and North
America.

Key findings/conclusions from our UK Van Duinen et al. Verberk et al. (2006) Mazerolle et al. Verberk et al. (2010) Hannigan et al. Elo et al. (2015)
study (2003) Netherlands(Verberk (2006) Netherlands(Verberk (2011) Finland(Elo et
Netherlands(Van et al., 2006) Canada(Mazerolle et et al., 2010) Ireland(Hannigan et al., 2015)*
Duinen et al., 2003) al., 2006) al., 2011)

Invertebrate taxonomic richness √ √

similar across pool types
Invertebrate community structure of √ √ √
restored peatland pools similar to
naturally-formed peat pools
Important habitats for diverse √ √ √ √
assemblages of Chironomidae
Coleoptera colonised restored √ √ √ √ √
peatland pools readily
Odonata populations establish in √ √ √ √ √ √
restored peatland pools
Potential benefits for organisms other √P √ Am, P
than invertebrates

Abbreviations: A – artificially-created pool on restored peatland; N – naturally-formed pool; P – plants; Am – amphibians; * Elo et al. (2015) study focused only on Odonata.

themselves are not restored (i.e. true restoration failure), or whether similarity of assembly processes in both restored and undisturbed
unanticipated outcomes are an inherent feature of stochastic assembly peatland pools could be generalizable. The characteristic low pH, low
processes creating different compositional end points (Lockwood and nutrient, waterlogged conditions of bog systems might also mean that
Pimm, 1999). In the latter, restoration might be classed as a failure restoration successfully recreates environments for re-establishment
owing to an ecological community composition not reaching a desired of ecological assembly processes in terrestrial ecosystem recovery.
goal, yet this might actually be a Type II error (false negative) because Significant amounts of money in the order of billions of dollars have
restoration has recreated the inherent stochasticity of the reference sys- already been directed to peatland restoration (Ramchunder et al., 2012;
tem. In systems characterised by more stochastic assembly processes, Cris et al., 2014) and our approach to evaluating community assembly
restoration practitioners might need to acknowledge this fundamental rules provides a new means of assessing the successful use of this
process (Lockwood and Pimm, 1999; Chase, 2007) and accept ‘success’ funding for biodiversity gains. More generally, the overall costs of eco-
once the ecosystem demonstrates an attainment of that state (i.e. ob- system restoration globally run into tens of billions of dollars each
served community not significantly different from null expectations, year (BenDor et al., 2015) but still a significant proportion of restoration
similar to reference system), even if community composition and biodi- schemes are deemed to be a failure (Benayas et al., 2009; Jones and
versity metrics remain different from the reference state. In a strongly Schmitz, 2009), often due to biodiversity goals not being met. Our dem-
deterministic system such as the dystrophic peatland pools we focused onstration of a new approach to evaluating restoration, that explicitly
on, there is a higher chance of restoration being deemed a success be- incorporates fundamental ecological theory, means that practitioners
cause community composition and biodiversity metrics are likely to can begin to evaluate the influence of assembly processes on the biodi-
converge on an end-point that is highly similar to the reference state. versity end-points reached after management interventions. Further
Restoration evaluations would therefore first need to determine the ex- development and incorporation of this approach into the planning,
tent of deterministic versus stochastic processes in the planning stages, goal setting and evaluation stages of ecological restoration has the po-
through the analysis of assembly processes in reference sites. This pro- tential to lead to a step change in the number of ecological restorations
cess-based information could be used subsequently to set realistic bio- deemed to be successful.
diversity goals for the restoration, and then evaluate post-restoration
community assembly processes against this reference site community
Author contributions
assembly benchmark.

Conceived of or designed study: LEB, JH, SJR.

5. Conclusions
Performed research: SJR.
Analysed data: LEB, SJR, JB.
Our results from UK peatland restoration schemes illustrate that
Wrote the paper: LEB, SJR, JB, JH.
there are strong similarities in terms of pool macroinvertebrate commu-
nity composition to peatland pool assemblages across other parts of Eu-
rope and North America (Table 3), where rewetting has also created Acknowledgements
vast new expanses of open water (Verberk et al., 2010; Hannigan et
al., 2011; Beadle et al., 2015; Elo et al., 2015). We have also demonstrat- This study was funded by an Esmée Fairbairn Foundation (10-0774)
ed how large-scale peatland restoration can be deemed successful for grant to LEB and JH. JMB's contribution was funded by a NERC student-
standing freshwater aquatic biodiversity, adding to earlier studies ship (NE/J50001X/1) with CASE support from the RSPB. The funders
showing benefits of these schemes for running water ecosystems played no role in study design, the collection, analysis and interpreta-
(Ramchunder et al., 2012). These biodiversity gains might have the po- tion of data, the writing of the report, or the decision to submit the arti-
tential to act as a further impetus, alongside existing carbon sequestra- cle for publication. We thank the landowners and gamekeepers for
tion targets, for businesses to invest in peatland restoration (IUCN allowing access to study sites. Garth Foster, APEM Ltd. and Steve Brooks
Peatland Programme, 2015). While our study is the first to address the kindly verified the identification of Beetle larvae and adults, non-chiron-
similarity of community assembly rules between restored peatlands omid taxa, and Chironomidae, respectively. Comments from three
and local reference conditions, the comparable community composition anonymous reviewers provided helpful suggestions that improved the
findings from a range of different northern peatlands suggest that the manuscript.
 L.E. Brown et al. / Science of the Total Environment 569–570 (2016) 361–372 371

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