Estuarine, Coastal and Shelf Science 68 (2006) 383e403www.elsevier.com/locate/ecss

Seagrass landscapes and their effects on associated fauna: A review

Christoffer Bostrom a,*, Emma L. Jackson b, Charles A. Simenstad c

a Environmental and Marine Biology, Abo Akademi University, Akademigatan 1, FIN-20500 Abo, Finlandb Marine Biology and Ecology Research Centre, Davy Building, Drake Circus, Plymouth, Devon PL4 8AA, UK

c School of Aquatic and Fishery Sciences, 324A Fishery Sciences, 1122 N.E. Boat Street, Box 355020, University of Washington,Seattle, WA 98195-5020, USA

Received 12 October 2004; accepted 23 January 2006

Available online 11 May 2006

Abstract

Seagrasses comprise some of the most heterogeneous landscape structures of shallow-water estuarine/marine ecosystems in the world. How-ever, while knowledge at the molecular, organism, patch and community scale is pervasive, understanding of seagrass landscape ecology is morefragmentary and has not been synthesized. The growth and recruitment dynamics of seagrasses as well as man-made and/or natural disturbancescreate complex spatial configurations of seagrass over broad (metres to kilometres) spatial scales. Hence, it is important to identify mechanismsmaintaining and/or threatening the diversity-promoting function of seagrass meadows and to understand their effects on benthic populations andcommunities. Although landscape ecology has recently become more integrated into seagrass research, our understanding of animal responses tovariability in seagrass landscape structure is still fragmentary. By reviewing the literature to date, this paper evaluates studies on seagrass land-scape ecology, testing the general null hypothesis that concepts developed in terrestrial settings can be generalized across landscapes, and (a)presenting definitions and terms used in seagrass landscape ecology, (b) reviewing geographical patterns of seagrass landscape studies to identifypossible key regions and target species, (c) evaluating different methodological approaches, (d) describing the spatial and temporal scales used todescribe organism responses to seagrass landscape structure, and (e) placing seagrass landscapes into an applied context.� 2006 Elsevier Ltd. All rights reserved.

Keywords: landscape ecology; seagrass; fragmentation; patch size; edge effects; perception

1. Introduction

It has become increasingly evident that adequate under-standing of local ecosystem processes requires considerationof expanding spatial scales. This mandate is predicated onthe premise that patterns (e.g., abundance, diversity, biomass)and processes (e.g., recruitment, predation, flows and produc-tivity) at a specific site can only be fully understood by includ-ing broad-scale (referring to larger areas, lower resolution andless detail, cf. fine-scale referring to small areas, greater reso-lution and more detail, sensu Turner et al., 2001) variables andlandscape attributes. In general, scaling issues, i.e. how

* Corresponding author.

E-mail address: christoffer.bostrom@abo.fi (C. Bostrom).

0272-7714/$ - see front matter � 2006 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ecss.2006.01.026

patterns and processes change with changes in scale, arecentral problems in ecology (Levin, 1992), in particular theconstraints of extrapolating phenomena that change discontin-uously with scale, i.e., the up-scaling of variables measured ata local scale (Wiens, 1989). Ecology, which tends to focus oninteractions among organisms and their environment at thefine-scale, can often predict species responses to local factorsat specific sites in homogenous environments, but is less effec-tive at predicting processes that operate over broader spatialscales. In contrast, landscape ecology focuses on ecologicalconsequences of broad-scale spatial heterogeneity and dynam-ics of biotic and abiotic processes over large areas (Formanand Godron, 1986).

The importance of scaling across landscapes has becomeparticularly germane while science is being required to guideecosystem restoration (Peterson and Lipcius, 2003; Bell et al.,

384 C. Bostrom et al. / Estuarine, Coastal and Shelf Science 68 (2006) 383e403

1997). Coastal management generally treats habitats sepa-rately, and there is no systematic understanding of the impor-tance of habitat location and connectivity. However,considering the spatial and temporal scales over which coastaldevelopment and other anthropogenic impacts occur, the mo-bility and dispersal range of marine organisms, and the broad-scale connectivity of many coastal habitats (e.g., seagrasses,saltmarshes, mangroves, oyster-, mussel- and coral reefs),unique approaches to research, management and restorationmust consider landscape scales in order to effectively assessthe effects of broad-scale patterns and changes in coastal eco-systems (Vidondo et al., 1997; Heck et al., 2003; Peterson andLipcius, 2003; Mumby et al., 2004).

1.1. Importance of seagrass landscapes

Seagrasses form unique, productive and highly diverse eco-systems throughout the world, and have been extensively stud-ied in some respects (e.g. their physiology and faunalassociations), during the last hundred years (Hemminga andDuarte, 2000; Short and Coles, 2001). On uniform substrates,such as bare sand or mud, seagrass patches (for definition ofa patch, see Section 3) provide physical structure with ecolog-ical functions that resemble mangroves, saltmarshes, and coraland oyster reefs (Sheridan, 1997). Seagrasses include <60species globally and their landscapes support high species di-versity by providing food, shelter and nursery areas for inver-tebrates and fish (Heck et al., 2003). A conservative estimateof the total area covered by seagrasses is 177,000 km2

(Spalding et al., 2003), and the economical value of all ecosys-tem services provided by seagrasses approaches US$3.8 tril-lion per year globally (Costanza et al., 1997). However,seagrasses are at a critical juncture. Heavily impacted by hu-man activities, about 12,000 km2 has been lost worldwide be-tween 1985 and 1995 (Short and Wyllie-Echeverria, 2000).

1.2. Aims of the study

Although responses of organisms and communities in terres-trial landscapes have been broadly reviewed (patch characteris-tics: Bender et al., 1998; Mazzerolle and Villard, 1999; habitatfragmentation: Harrison and Bruna, 1999; Fahrig, 2003), ourunderstanding of the response of seagrass landscape associatedspecies and communities to variability in seagrass landscapestructure and dynamics is still fragmentary (Bell et al., 2001).

Firstly we review landscape patterns and processes thatcause them, and then present models for faunal distribution.Then we review and evaluate studies on seagrass landscapeecology, testing the general null hypothesis that concepts de-veloped in terrestrial settings can be generalized across land-scapes, and presenting (a) definitions and terms used inseagrass landscape ecology, (b) geographical patterns of sea-grass landscape studies to identify possible key regions andtarget species, (c) different methodological approaches, (d)the spatial and temporal scales used to describe organism re-sponses to seagrass landscape structure, and (e) place seagrasslandscapes into an applied context.

In this process, we asked the following questions: (1) Whatare the advantages and/or limitations/constraints of applyingconcepts of terrestrial landscape ecology to study seagrass eco-systems? (2) What is the relative importance of broad-scale het-erogeneity (landscape structure) compared to local-scalecomplexity (patch structure) for ecosystem structure and func-tion? (3) What organism responses to landscape patterns havebeen documented, and how do they vary over organismal, tem-poral and spatial scales? (4) What are the proposed mechanismsof responses? (5) What kind of conservation and restorationstrategies does the present knowledge suggest, and how shouldseagrass landscape ecology be incorporated into management?

1.3. Mechanisms causing spatial heterogeneity inseagrass landscapes

The spatial heterogeneity and dynamics of seagrass land-scapes are driven by internal regulatory mechanisms and ex-ternal demographic events and environmental factors(Frederiksen et al., 2004). Hence, in order to discriminate be-tween human impacts and natural landscape patterns and dy-namics, a thorough understanding of both the basicautoecology of the landscape-forming species and the physicalsetting is required (Kelly, 1980; Fonseca and Bell, 1998). Re-cruitment and growth patterns in seagrasses can occur by bothsexual (flowering and seed dispersal) and asexual (vegetativepropagation) processes, but their relative importance of thedifferent regulatory mechanisms is scale dependent. Giventhat fauna respond to spatial heterogeneity in seagrass land-scapes, it is critical to understand the scales of ecosystem pro-cesses that shape seagrass landscapes before we can inferfaunal responses. It is beyond the scope of this review to pro-vide a detailed review of all factors underlying patch forma-tion, growth and mortality of different seagrass species, butit is important to at least distinguish regulatory mechanismsinternal and external to seagrass patches. Although we recog-nize that seagrass landscapes can be characterized by manyvariables, we focus on areal cover because that is the most uni-versal metric of seagrass heterogeneity in the literature.

1.4. Internal regulatory mechanisms

The main internal factors driving space occupation inclonal plants such as seagrasses are species specific, and aredetermined by rhizome elongation rates (primarily through ac-tive cell division in the meristemal region), and the probabilityand angle of branching of the rhizomes (Duarte and Sand-Jensen, 1990a,b). Sediment texture and chemistry (nutrientavailability), light availability and inter- and intra-specificcompetition are prominent controls on small-scale (cm-m) lat-eral expansion of seagrass patches by rhizome elongation ofterminal shoots at the patch margins (Marba and Duarte,1998; Hemminga and Duarte, 2000), and are especially welldocumented for Posidonia spp. (Marba et al., 1996; Kendricket al., 1999; Meehan and West, 2004), Cymodocea nodosa(Duarte and Sand-Jensen, 1990a,b; Marba and Duarte, 1994;Marba et al., 1994; Marba and Duarte, 1995) and Zostera

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spp. (Olesen and Sand-Jensen, 1994a,b; Turner et al., 1996;Ramage and Schiel, 1999).

Patch growth is centrifugal and self-accelerating, which isresponsible for asymmetry in patch shape, exponential increasein shoot density with increasing patch age, and increased patchformation rates over time. Thus, the capacity of seagrasses tooccupy space by clonal growth is a key factor in appearance, de-velopment and maintenance of seagrass landscapes. However,there is considerable variation among species in terms of rametelongation rates (1e500 cm yr�1) and patch formation ratesfrom seeds, e.g. Posidonia oceanica: <5, Cymodocea nodosa:w50 and Zostera marina patches >5000 patches ha�1 yr�1

(see Hemminga and Duarte, 2000, and references therein).This implies that seagrass recruitment and growth processescounteracting seagrass landscape fragmentation or loss arenot constant or uniform among species, but increase throughtime and occur over shorter time scales than predicted frommodels (Hemminga and Duarte, 2000; Kendrick et al., 2005).

In contrast, spatial variation in sexual reproduction and dis-persal by seed production and seedling recruitment are stilllargely ignored research topics (Orth et al., 1994). Formationof new patches outside existing meadows by sexual propagulesor drifting rhizome fragments is a rare event due to high seed-ling mortality (e.g., Duarte and Sand-Jensen, 1990a; Orthet al., 2002; Paling et al., 2003). Seed dispersal and survivalalso vary due to stochastic events (see below), and pollen dis-persal is assumed to be limited to the extent of meadows them-selves, i.e., <30 m (Orth et al., 1994, 2000; Ruckelshaus,1996). Seed survival may also show distinct within-patchand between-patch patterns. For example, isolated patchesshow lower seed set compared to continuous patches (Reusch,2003) and rates of seed predation differ inside compared tooutside seagrass patches, although not always in the same di-rection (Heck and Crowder, 1991; Orth et al., 2002). Since ge-netic attributes partly determine reproductive output, and thusdispersal capacity (pollen availability and gene flow) andpatch formation at the local scale, with considerable implica-tions about patch age and resistance to disturbance (Hughesand Stachowicz, 2004; Rhode and Duffy, 2004), they shouldalso be considered in seagrass landscape ecology.

Covariation of local, within-patch structure with landscapestructure can obscure the actual mechanism responsible forpatch dynamics, as well as the scale of factors underlyingfauna responses (see below). This may particularly be thecase where increased plant density corresponds to areal expan-sion of patches during early colonization (Worm and Reusch,2000). Plant performance in some seagrass species can vary byposition of the plant position in the patch, with higher shootdensity, above-ground biomass, and leaf area index at the cen-tre of the patch (Brun et al., 2003).

1.5. External regulatory mechanisms

Although some local-scale attributes, such as shoot mortal-ity and recruitment may vary over broad, even regional, scales(e.g., Marba et al., 2005), variation in landscape structure suchas sizes, shapes and distributions of patches is driven more by

abiotic or disturbance (including biotic) factors. Patchiness ismaintained through external factors, mainly hydrodynamic ac-tivity and the underlying geomorphology of the area. Seagrasslandscapes at high-energy sites change through time (Fonsecaand Bell, 1998), but can exist in a dynamic equilibrium be-tween clonal growth and spatial fragmentation depending onthe disturbance frequency and amplitude (Duarte, 1991).This results in more homogeneous landscapes in low-energyenvironments, and heterogeneous, patchier landscapes in envi-ronments structured by currents, waves, sedimentation eventsand wind (Den Hartog, 1971; Patriquin, 1975; Fonsecaet al., 1983, 2000; Fonseca and Fisher, 1986; Fonseca andBell, 1998; Bell et al., 1999; Frederiksen et al., 2004). Instrong current regimes this reticulated pattern is exaggeratedvia mounding (differences in sediment height between sea-grass [higher] and unvegetated regions [lower]). This turretedprofile is thought to be the result of increased deposition andbinding of sediment by the rhizomes where there is seagrass,combined with increased, channelled current strength betweenseagrass patches (Patriquin, 1975; Kelly, 1980; Fonseca et al.,1983; Ward et al., 1984). Water depth can modulate factorssuch as exposure and local current speeds, thereby influencingseagrass landscapes (Robbins and Bell, 2000; Koch, 2001).The effects of wave exposure are more pronounced when shal-low-water waves (depth < half the wave length) can form(Fonseca and Bell, 1998). Depth may also have a more indirectinfluence on seagrass landscape configuration perhaps relatingto light attenuation coefficients (Duarte, 1991, see below). Insummary, much of the available evidence points to a closecoupling between near shore hydrodynamic and geologicalprocesses. Both strongly influence the patterns, dynamicsand long-term development of seagrass landscapes.

Covariation of landscape-scale structure driven by externalfactors with internal factors regulating local-scale patch vari-ability can complicate inference about the scale of faunal re-sponses, and may even be driven by processes beyondlandscape scales (Hovel et al., 2002). For instance, the re-sponse of some fauna, especially less motile benthic inverte-brates, may vary more with local-scale patch characteristicssuch as shoot density and above-ground biomass (althoughnot necessarily below-ground biomass, Webster et al., 1998)than to landscape-scale patch variation (Irlandi, 1997; Salitaet al., 2003).

1.6. Human-induced changes in seagrass landscapes

Of considerable management concern is the multitude ofanthropogenic factors that affect seagrass landscapes. In a studyidentifying the environmental impacts on the Posidoniameadows along the Corsican coast, Pasqualini et al. (1999) il-lustrated changes to the configuration of the patches at a land-scape scale due to various human activities (trawling,anchoring, bomb blasts). Boat anchoring (Francour, 1999),propeller scarring (Bell et al., 2002; Uhrin and Holmquist,2003), dredging and destructive fishing methods such asbeam trawling (Sanchez-Jerez et al., 1999), have all beenshown to physically damage seagrasses (De Jonge and

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De Jonge, 1992). While many of these activities tend to havea localized impact, permanent moorings and bomb damageresult in the fragmentation of the seagrass landscapes in a verydifferent way than dragged anchors, mobile gear or dredging,by creating small patches of bare sand in a matrix of seagrass,rather than unvegetated channels dissecting contiguous sea-grass into separate patches (see Fig. 2 in Pasqualini et al.,1999). Other anthropogenic pressures that impact seagrassesmay not be immediately or directly observable at the land-scape level. Activities which decrease water clarity or quality(for example eutrophication, aquaculture, coastal develop-ment, dredging, spoil disposal) may negatively impact thehealth or productivity of the seagrass, but only in extremecases or after continued exposure, manifest themselves at thelandscape scale (Pergent et al., 1999; Ruiz and Romero,2003). Increased turbidity may reduce the depth limit andthus vertical distribution of the seagrasses and the shape ofseagrass patches (Frederiksen et al., 2004). In addition, phys-ical disturbance from animal feeding activities and bioturba-tion (Thayer et al., 1984; Townsend and Fonseca, 1998), icescouring (Robertson and Mann, 1984), disease pathogens(Ralph and Short, 2002) and algal mats (Cowper, 1977) arealso important disturbance factors in many seagrassecosystems.

1.7. Models explaining faunal distributions

Effects of broad-scale spatial heterogeneity have tradition-ally been studied in terrestrial systems (Forman and Godron,1986). But, landscape ecology has been found equally applica-ble to the study of heterogeneity in marine (e.g. Paine andLevin, 1981; Keough, 1984; Sousa, 1984; Scheltema, 1987;Bell and Hicks, 1991; Sebens, 1991; Goodsell and Connell,2002; Teixido et al., 2002) and freshwater (Johnson andGage, 1997) ecosystems. Robbins and Bell (1994) were prob-ably the first to describe that patchy seagrass landscapes pro-vide promising systems for testing models developed interrestrial landscapes. Like terrestrial landscape ecology, theecological study and quantification of seagrass landscapeshas been influenced by two main perspectives, the island bio-geography model and the landscape mosaic model (MacArthurand Wilson, 1967). Island biogeography models suggest thatthere is a focal habitat patch type (seagrass), which occursin a matrix of a less favourable or ‘‘ecologically neutral’’ hab-itat (e.g., unvegetated substrate), analogous to oceanic islands(Haila, 2002). Although seagrass landscape studies do not in-corporate the long time scales inherent in the island biogeog-raphy model, the majority of seagrass landscape studies arebased on these models, which encompass studies of fragmen-tation and patch dynamics (Table 1).

Taking into account that organisms rarely show a preferencefor a specific structured habitat, i.e. seagrass, oyster reefs,macroalgae and mangrove, an alternative view is to see thespecies/process/question-specific landscape as a mosaic of dif-ferent habitats (McGarigal and Cushman, 2002) which pro-poses that optimal foraging/movement and fitness strategiesvary for different animals within a mosaic.

Other models partly developed from the island biogeogra-phy model but not yet broadly applied to marine systems in-clude: (1) metapopulation models (Hanski and Gilpin, 1997)which focus on patchy habitats, but emphasize the importanceof dispersal between isolated fragments, assuming a networkof patches without a persistent mainland and focusing on thedynamics of usually single species. Species interactions havebeen considered in so-called (2) metacommunity models (Har-rison and Taylor, 1997), which emphasize the importance ofpredatoreprey interactions and competition. (3) Sourceesinkmodels (Pulliam, 1988) are related to fragmented habitatsand emphasize the importance of patch quality for animalmovement patterns. Fragmentation is closely integrated with(4) percolation theory, where a fragmented landscape inhibitsthe ability of organisms to move across/through landscapes(Wiens et al., 1997).

2. Methods

Seagrass landscape ecology is methodologically and the-matically a diverse field, utilizing diverse methodological ap-proaches, e.g., field surveys, transplantations, artificialsubstrates, remote sensing and GIS, and targeting differentfaunal (meiofauna to megafauna) and floral groups overwide spatial (millimetres to thousands of kilometres) and tem-poral (hours to millennia) scales. To delineate our review, weused the work by Robbins and Bell (1994) as a landmark pa-per, since they were the first authors to apply principles andtechniques developed in terrestrial landscape ecology to studyseagrass ecosystems. To summarize how this field has devel-oped, we evaluate all the literature dealing with the responseof animal communities to seagrass landscapes that has beenpublished in international peer-review journals during thetime-period 1994e2004. In addition to personal libraries, weused Cambridge Scientific Abstracts and Biblioline (NISCInternational, 2004) to identify papers containing the key-words ‘‘seagrass’’ and the following indicators of a landscapeapproach: ‘‘landscape’’, ‘‘patch size’’, ‘‘corridor’’, ‘‘edge’’,‘‘fragmentation’’, ‘‘patchiness’’, ‘‘habitat mosaic’’ and ‘‘artifi-cial’’ in the title or abstract.

To summarize general tendencies across seagrass landscapestudies (for species-specific responses of nekton to landscapestructure and methodological aspects, see Connolly and Hin-dell, this issue), we used as a metric the proportion of studiesreporting significant (P � 0.05) and non-significant (P> 0.05)results, without taking into account the statistical power ofindividual studies (cf. Mazzerolle and Villard, 1999). To detectpossible effects of patch and landscape variables on the mostcommonly reported faunal groups and/or processes we alsoused the total number of significant results, because many pa-pers reported significant or non-significant results for severaldifferent sampling occasions and/or for several taxa.

Although the focus was planteanimal interactions in sea-grass landscapes, we included some studies focusing on otherlandscape forming vegetation (e.g., saltmarshes) only if sea-grasses were included and played a critical role for the out-come of the study. Aerial photography often provides the

Table 1

Compilation of studies (1994e2004) dealing with planteanimal interactions in seagrass landscapes. MFS, manipulative field study; DFS, descriptive field study; ASU, artificial seagrass unit. Explanatory variables

asurement of above- or below-ground structural

on, juxtaposition etc. Patch quality refers to food

(h, hours; d, days; wks, weeks; mo, months; yrs,

Source

al and siphon weights

reater energy transfer

re economically

Irlandi (1994)

ing seagrass cover.

h cover. Spatial

ass, alters predation

ergy transfer from

orridors facilitating

Irlandi et al. (1995)

st in medium patches.

d large patches,

independently of

sites.

Irlandi (1996)

by the adjacent

djacent to seagrass

e substrate. Higher

ss beds. Marsh/mudflat

sh/seagrass boundaries.

Irlandi and

Crawford (1997)

e biomass increased

ht times higher in small

cts of when shoot density

Irlandi (1997)*

small than in

nd life-stage specific

of seagrass.

Eggleston

et al. (1998)

ods higher in small

ial pattern dependent

y size. Between site

atch size.

Eggleston

et al. (1999)*

edium and small

equivocal and

ith growth period,

edation rates only

t over longer

Irlandi et al.

(1999)

to seagrass beds than

as corridors facilitating

g landscape components

Micheli and

Peterson (1999)

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refer mainly to parameters related to landscape pattern, (although studies include other explanatory and/or environmental variables). Complexity refers to any me

complexity (e.g. shoot density, shoot length, leaf width, above-ground biomass or below-ground biomass). Configuration includes fragmentation, adjacency, isolati

resources in terms of epiphytes. Response parameters refer to those reported for target animal groups, not vegetation. Time span refers to duration of study period

years). Depth refers to the depth at which the study was conducted. Studies marked with an asterisk (*) were not temporally replicated

Latitude/longitude Study

type

Vegetation Explanatory

variables

Target

taxon

Response

variable

Time

span

Depth

(m)

Conclusions

USA

North Carolina

35 �420 N, 76 �360 W MFS Z. marina Cover (%) Bivalves Biomass wk <1.5 Shoot density and biomass, clam surviv

increased with decreasing patchiness. G

from patchy beds since they support mo

important predator species.

H. wrightii Configuration Mortality

Complexity

35 �400 N, 76 �350 W MFS H. wrightii Cover (%) Bivalves Growth dewk <1.5 Scallop survival decreased with decreas

Seagrass parameters did not change wit

pattern, independent of density and biom

rates and foraging strategies. Higher en

patchy habitats. Bare sand function as c

predator movement.

Z. marina Configuration Predation

Complexity Mortality

35 �400 N, 76 �350 W MFS Z. marina Patch size Bivalves Biomass mo <1.5 Shoot density lowest in small and highe

Large clams grew fastest in medium an

intermediate in small. Small clams grew

patch size and varied >5 times among

Complexity Body size

Growth

35 �420 N, 76 �360 W DFS H. wrightii Configuration Fish Density hemo <1.5 Movement from marsh edges influenced

habitat. Greater growth in marsh areas a

than in marsh habitats adjacent to a bar

fish densities in marshes close to seagra

boundaries less permeable than the mar

MFS Z. marina Edge effects Growth

Complexity Movement

35 �420 N, 76 �360 W DFS Z. marina Patch size Bivalves Mortality mo <1.5 Clam survival, shoot density and rhizom

with increasing patch size. Survival eig

patches than in sand. No patch size effe

was held constant using ASUs.

MFS R. maritima Complexity

ASU H. wrightii

34 �400 N, 76 �300 W MFS No Patch size Shrimps Crabs Density wk <1.5 Significantly higher shrimp densities in

intermediate and large ASUs. Species a

responses to spatial pattern (patch size)

ASU

34 �400 N, 76 �300 W MFS No Patch size Epifauna Density wk <1.5 Density of shrimps, amphipods and isop

than in large patches. Responses to spat

upon spatial scale, habitat type and bod

variability larger than variation due to p

ASU Complexity Infauna No. of spp.

Body size

Funct. group

35 �400 N, 76 �300 W MFS Z. marina Patch size Bivalves Growth mo <1.5 Higher shoot density in large than in m

patches. Effects of patch size on growth

dependent on food supply which vary w

season and site. Patch size effects on pr

evident over short (24 h) periods, but no

(2e7 weeks) time periods.

ASU H. wrightii Complexity Condition

Mortality

35 �420 N, 76 �350 W DFS Z. marina Configuration Bivalves Movement d <1.5 Crab predation higher on reefs adjacent

on isolated reefs. Vegetated habitats act

predator movements. Connections amon

important.

MFS H. wrightii Corridors Mortality

Table 1 (continued)

Latitude/longitude Study

type

Vegetation Explanatory

variables

Target

taxon

Response

variable

Time

span

Depth

(m)

Conclusions Source

agrass biomass and animal

fects on abundance, and

number. Hydrodynamics

r faunal density. Interacting

th landscape structure.

Hovel et al. (2002)

ch variables in both

l and patch size not

effects differs between

plexity and

Hovel (2003)

mpared to unvegetated

ition of mussels inside

ide vegetation and

No effect of patch size

Reusch and

Williams (1999)

compared to edges, but

l density, but not

rior parts, and varied

dates. Mostly (4 of

at edge than in

Bologna and

Heck (2002)

than along edges. Scallops

her growth rates, but lower

s. Predation stronger along

Bologna and

Heck (1999a)

ges compared to interiors,

r time. A general positive

and density, but size

ried with sampling date

s enhanced bivalve

Bologna and

Heck (2000)

and patch size. Amphipod

owed positive relationship

ng. One polychaete

interior parts than

Bell et al.

(2001)

a among seagrass

patch edges had higher

moved within patches or

among ontogenetic stage

Brooks and Bell

(2001)

d predator density in ASUs

to controls. Artificial

ing bivalves. Food

on ratios.

Bologna and

Heck (1999b)*

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34 �450 N, 76 �300 W DFS Z. marina Cover (%) Shrimps Density yr <1.5 High spatio-temporal variability in se

density. Landscape variables weak ef

related only to crabs, fish and species

and shoot biomass more important fo

processes limit faunal correlations wi

R. maritima Configuration Crabs Body size

H. wrightii Complexity Fish

California, N. Carolina

38 �200 N, 123 �030 W DFS H. wrightii Cover (%) Crabs Mortality hed <1.5 Shoot density did not correlate to pat

regions. Correlations between surviva

consistent among regions. Patch size

regions due to interacting effects com

hydrodynamics.

34 �420 N, 76 �340 W MFS Z. marina Patch size

Configuration

Complexity

California

32 �430 N, 117 �110 W MFS Z. marina Patch size Bivalves Density wkemo <1.5e3.5 Mussel growth inside eelgrass half co

areas. Lower survival and worse cond

vegetation. Growth rates highest outs

decreased with increasing patch size.

on shoot density.

Configuration Condition

Edge effects Growth

Complexity

Florida

29 � N, 85.5 � W DFS T. testudinum Edge effects Epifauna Density mo <1.5 Higher plant biomass in interior parts

no differences in flow regime. Fauna

biomass, greater at edges than in inte

among individual taxa and sampling

5 dates) higher secondary production

interior locations.

MFS S. filiforme Complexity Infauna Biomass

H. wrightii Production

29 � N, 85.5 � W MFS T. testudinum Edge effect Bivalves Growth dewk <1.5 Higher shoot density in interior parts

were more abundant and showed hig

survival at edges than in interior part

edges than in sand and seagrass.

S. filiforme Complexity Predation

H. wrightii Mortality

29 � N, 85.5 � W DFS T. testudinum Patch size Bivalves Density moeyr <1.5 Greater density and richness along ed

but this pattern was not constant ove

relationship between patch perimeter

and shape effects inconclusive and va

and ASU deployment time. Epiphyte

settlement.

MFS H. wrightii Patch shape Composition

ASU S. filiforme Patch quality No. of spp.

Edge effects Recruitment

27 �470 N, 82 �370 W DFS H. wrightii Patch size Fish Density moeyr <1.5 No relationship between fish density

density, but not individual species, sh

with patch size in fall but not in spri

species exhibited higher densities in

along edges.

Edge effect Epifauna

Infauna

27 �36 N, 82 �46 W MFS H. wrightii Edge effects Epifauna Density d <1.5 Drift algae enhance dispersal of faun

patches. Algal clumps moved across

abundances of amphipods than algae

over bare sand. Movements differed

and sex.

T. testudinum Corridors Sex

Movement

29 � N, 85.5 � W MFS T. testudinum Patch quality Epifauna Density wk <1.5 Higher species richness, epifaunal an

with epiphytes community compared

epiphytic structure important for settl

resources affect immigration/emigrati

ASU S. filiforme No. of taxa

H. wrightii

Virginia

37 �130 N, 76 �240 W DFS Z. marina Patch size Crabs Density d <1.5 Early summer: increasing crab survival with decreasing patch

ity in small patches.

ot density regardless

rvival varied temporally.

bitats.

Hovel and

Lipcius (2001)

and small patches

not correlated to

her in connected

orrelated with

correlated with

ll patches compared

arts compared to

Hovel and

Lipcius (2002)

patch size. Mussel

red to bare sand, and

in medium sized

Reusch (1998)*

infauna was the same

ifferences in

sorted sediment in

the same in both bed

w50% of the

Frost et al.

(1999)*

rge patches higher

han small, but not

relationships and

onses species/taxa

nexplained.

Bowden et al.

(2001)*

epended on time of

xcept mysids,

es.

Sanchez-Jerez

et al. (1999)

nsities and species

ous. Density highest

segregation by

Barbera-Cebrian

et al. (2002)

ing patch size at

r predator density,

patch size at both

Laurel et al.

(2003)

(continued on next page)

38

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size, possible due to lower predator dens

Late summer: survival increased with sho

of patch size. Fragmentation and crab su

Trend for lower survival in connected ha

MFS Configuration Mortality

ASU Complexity

37 �130 N, 76 �240 W DFS Z. marina Patch size Crabs Density dewk <1.5 Shoot density differences between large

varied over the season. In June, survival

patch size and shoot density and was hig

patches. In September survival was not c

patch size and connectivity, and inversely

shoot density. Higher crab density in sma

to larger. Density was higher in interior p

edges.

MFS Configuration Body size

Edge effects Mortality

Complexity

Germany

Baltic Sea

54 �410 N, 10 �000 E MFS Z. marina Patch size Bivalves Growth mo 1.5e3 Both enhancing and depressing effects of

growth reduced by 2/3 in patches compa

independent of patch size. More recruits

patches than in small and large patches.

Complexity Recruitment

UK

South west

50 �140 N, 3 �460 E DFS Z. marina Configuration Infauna Density d <1.5? Density, number of taxa and diversity of

in fragmented and continuous beds, but d

community composition. Finer and well

continuous bed, but the silt fraction was

types. Sediment characteristics explained

community structure.

Complexity No. of taxa

Diversity

49 �570 N, 06 �190 W DFS Z. marina Patch size Infauna Density d <1.5 Higher shoot density in interior parts. La

percentage of fines and number of taxa t

higher diversity and density. Species-area

edge vs. interior effects present, but resp

specific. 60% of the infaunal variability u

Edge effects Composition

Complexity No. of spp.

Diversity

Spain

Alicante

38 �200 N, 00 �300 W DFS P. oceanica Configuration Epifauna Density mo 5e10 Importance of Posidonia meadow edge d

year and taxa. Most taxonomic groups, e

showed no clear response to meadow edg

C. nodosa Edge effects

38 �200 N, 00 �300 W DFS P. oceanica Edge effects Mysids Density moeyr 5e10 Fragmented habitats supported higher de

richness of mysids compared to homogen

at Posidonia edges. Three species showed

habitat.

C. nodosa Configuration

Canada

Newfoundland

48 �570 N, 53 �920 W MFS Z. marina Patch size Fish Predation mo-yr 1.5e3.5 Increasing predator densities with increas

both sites. In <11 m2 patches with simila

predation rates increased with decreasing

sites each year.

ASU Mortality

Table 1 (con

Latitude/lon Source

The Philipp

Bolinao

15 � S, 120 � more important than patch shape for

nships between density and habitat

abundances in fragmented and

ntermediate levels of patchiness

aried temporally and when absent,

portant than configuration.

Salita et al.

(2003)

New Zealan

37 �020 S, 17 l component more important

nment. Patch variables explained

l component 14% of the variation.

e important than patch scale

landscape scale, wave exposure

variation. Lower seagrass biomass

Turner et al.

(1999)

Australia

Gulf St. V

34 �450 S, 13 but fish decreased in patches

rrent. Amphipods (but not fish)

esponses to shape. Edge length

t more important than patch

ited adult dispersal showed no

e or orientation.

Tanner (2003)

34 �170 S, 13 mass at the edge. Epifauna

effects than infauna. Crustacean

e not consistent among sites.

s showed consistent peaks in

. Predation important mechanism.

lity unexplained.

Tanner (2004)*

39

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tinued)

gitude Study

type

Vegetation Explanatory

variables

Target

taxon

Response

variable

Time

span

Depth

(m)

Conclusions

ines

E DFS T. hemprichii Cover (%) Fish Density mo <1.5 Continuity of patches

fish. Non-linear relatio

heterogeneity (highest

continuous seagrass). I

avoided. This pattern v

shoot density more im

C. rotundata Patch size Body size

Patch shape

Configuration

Complexity

d

4 �410 E DFS Z. novaze-landica Cover (%) Infauna Density moeyr <1.5 At patch scale tempora

than that of the enviro

<4% and the tempora

Landscape pattern mor

characteristics. At the

explained 62% of the

in larger patches.

Patch size Composition

Configuration No. of spp.

Complexity Sp. richness

Diversity

Evenness

incent

8 �300 E MFS No Patch shape Fish Density wkemo <1.5 Amphipods increased,

perpendicular to the cu

showed taxa-specific r

perpendicular to curren

shape. Groups with lim

response to patch shap

ASU Configuration Epifauna Composition

Infauna No. of taxa

8 �010 E DFS Z. muelleri Configuration Epifauna Density mo <1.5 Maximum seagrass bio

showed stronger edge

responses to patch edg

Amphipods and tanaid

abundance at the edge

Much infaunal variabi

Z. macronuta Edge effects Infauna

Complexity

391C. Bostrom et al. / Estuarine, Coastal and Shelf Science 68 (2006) 383e403

basis for quantifying seagrass landscapes, but we excluded lit-erature dealing with mapping and monitoring of seagrassesthrough satellite and aircraft remote sensing. In order to com-pare results from studies using artificial seagrass units (ASUs;Bell et al., 1985), we excluded those employing ASUs con-structed with any above-ground structure other than plasticleaves, such as concrete moulds, trays or frames (e.g., Kenyonet al., 1999; Bostrom and Bonsdorff, 2000; Bartholomew,2002).

3. Results

3.1. Geographical key regions, target seagrass speciesand methodological approaches

A total of 33 papers published between 1994 and 2004 metour search criteria (Table 1). The majority (w80%) of paperswere published during the second half of this ten-year period,with a peak in 1999. Considering a publication rate in seagrassecology of >100 papers per year (Hemminga and Duarte,2000), the landscape ecological literature focusing on planteanimal interactions contribute but <3% to the research fieldeach year. The geographical distribution of these studies isskewed towards the temperate northern latitudes, with two-thirds of all studies being conducted between 30 � N and 40 �

N. This distribution corresponds to the latitudinal range withthe lowest global seagrass species diversity. The longitudinalpattern is skewed toward west, with >50% of all studies con-ducted between 75 � W and 100 � W. Over 60% of all studieshave been carried out in the United States (US), of these 85%were conducted in North Carolina or Florida. Less than 20%of the studies have been carried out in Europe, and workfrom the southern hemisphere contributed <15% (Table 1).

Consequently, the distribution of study areas is reflected inthe seagrasses investigated, with Zostera spp., Halodulewrightii, Thalassia spp. and Syringodium filiforme being themost studied landscape-forming genera/species (Fig. 1a).Notably, landscape effects on associated organisms is poorlyknown for the key seagrass species of southern (Posidoniaoceanica and Cymodocea nodosa) and northern (Zosteraspp.) Europe (Sanchez-Jerez et al., 1999). About 30% of thestudies were purely descriptive field studies, while 70% in-cluded a manipulative approach. ASUs were used in 40% ofthe manipulative field studies, and ranged in size between0.01 and 22 m2, the most frequently tested sizes being 1(w25%) and 4 m2 (w15%), respectively. About 30% of thepapers combined a descriptive and manipulative approach.Over 80% of the studies selected for this review focused onseagrass landscapes occurring at depths less than 150 cm(Table 1). No laboratory or mesocosm study matched oursearch criteria. All studies involved spatial replication ofsamples or experimental units, but the scale of the samplingarea was highly variable. If several sites were included theywere usually several kilometres apart. If a mosaic of naturalpatches was studied, the area ranged between <100 m2 to>3000 m2. Two-thirds of the papers included a temporal as-pect either in terms of repeated sampling or repetition of an

experimental manipulation. The time span of studies washighly variable ranging from a few hours to several years,and most studies typically lasted from a few days or weeksto several months.

3.2. Landscape variables

The definition of a seagrass patch is dimensionless andneeds to be defined relative to the question being asked orthe organism under study (Table 2). Seagrass patches

0 20 40 60 80 100

Mortality

Growth

Predation

Movement

Recruitment

Production

Density

No. of species/taxa

Composition

Biomass

Diversity

Other c

d

Bivalves

Epifauna

Infauna

Fish

Crabs

Shrimp b

Zostera spp.

H. wrightii

Thalassia spp.

S. filiforme

Cymodocea spp.

Posidonia spp.

R. maritima a

Percent of studies

Fig. 1. Proportional representation of response variables in terms of seagrass

species (a), faunal groups (b) community parameters (c), and biotic processes

(d) to seagrass landscape structure in the studies examined (1994e2004).

392 C. Bostrom et al. / Estuarine, Coastal and Shelf Science 68 (2006) 383e403

Table 2

Definitions of terms used in landscape ecological seagrass studies

Term Synonyms Definition Source

Seagrass

landscape

Seascape A landscape is an interacting mosaic of patches relevant to the

phenomenon under consideration (at any scale), characterized

by both its composition and configuration.

McGarigal et al. (2002)

Seagrass mosaic

Patch Bed (1) Distinct areas with habitat conditions different from the surrounding

areas as perceived by the organism under study or from the point of view

of management objectives. (2) Territorial unit, which represents an area

covered by one single land cover class. (3) Relatively homogeneous non-linear

area that differs from its surroundings. The internal microheterogeneity present

is repeated in similar form throughout the area of a patch.

Forman (1995), European

Commission (2000), McGarigal

et al. (2002)

Habitat

Component

Element

Matrix Dominant

habitat

(1) The most extensive and most connected landscape element type.

(2) Element that plays the dominant role in the functioning of the landscape.

(3) Background ecological system, characterized by expanded surface covering,

high connecting degree and/or main control of the landscape dynamics.(What

constitutes the matrix is dependent on the scale of investigation or management)

Forman (1995), McGarigal

et al. (2002)

Gap Halo, Space Patch elements of one habitat within a matrix of another. From a seagrass

landscape perspective this is usually a patch of unvegetated substrate in a

matrix of seagrass.

Patriquin (1975), Sousa (1984)

Blow out

Corridor Linkage (1) Vegetated or unvegetated strip between patches facilitating faunal dispersal

and movement. (2) ‘‘Mobile corridor’’ for drifting algae moving in a seagrass-sand

mosaic. (3) A linear strip of suitable habitat (as perceived by the organism) which

allows movement between preferential habitat patches.

Adapted from Micheli and

Peterson (1999), see also Brooks

and Bell (2001)

Artificial

seagrass unit

ASU An artificially made seagrass patch, with standardized area, shoot density, shoot

length, leaf width, usually constructed by plastic ribbon tied to a coarse plastic

mesh.

Bell et al., 1985

Artificial plot

Habitat

fragmentation

(1) This term describes a generally gradual phenomenon marked by the rupture

of certain linkagesda reduction in connectivity among ecosystems in a given

landscape. (2) The breaking up of habitat into smaller somewhat-widely and

usually unevenly separated parcels, usually also including spatial configuration

of the resulting patches. (3) Changes in habitat configuration that result from

the breaking apart of habitat, independent of habitat loss.

Forman (1995), Aronson and

Le Floc’h (1996), Fahrig (2003)

Edge Ecotone (1) A region of change from one habitat to another as perceived by the organism

under consideration. Unfortunately this is often at the scale that can be

differentiated by mapping software. (2) The portion of an ecosystem near its

perimeter, where influences of the surroundings prevent development of interior

environmental conditions. (Edge effect refers to the distinctive species composition

or abundance in this outer portion.) (3) When the landscape is represented as a

mosaic of qualitatively different types, edges are defined as the location where

two types adjoin. When a landscape is represented as a continuum in amount or

intensity of some variable, one solution is to define edges as the points where

the local gradients exceeds some threshold.

Turner and Gardner (1991),

Forman (1995)Ecocline

Boundary

embedded in an unvegetated matrix have distinct boundaries.Hence, in contrast to terrestrial patches, no criteria to distin-guish patches are usually needed. However, although the tech-nical definition of a patch is straightforward, i.e., ‘‘acontinuous (non-linear) surface area differing from its sur-rounding in terms of habitat type, heterogeneity, boundarycharacteristics, size and shape, and containing all necessary re-sources for the persistence of a local population’’ (Hanski andSimberloff, 1997), there exists a confounding/inconsequentuse of terms such as ‘‘stand’’, ‘‘clump’’, ‘‘bed’’ and‘‘meadow’’ in the seagrass landscape literature. Hence, anarea covered by seagrass may be defined as a ‘‘meadow’’ or‘‘bed’’ by some workers and as a ‘‘patch’’ by other workers.Consequently, the size of discrete vegetated areas hereafter de-fined as ‘‘patches’’ varies widely in the literature; the mostcommonly size range being approximately 10e100 m2. Thesmallest and largest areas defined as seagrass patches were0.3 and >3000 m2, respectively (Fig. 2a,b).

In terms of patch characteristics, 50% of the papers exam-ined the role of patch size and 43% examined edge effects, i.e.,possible differences in response variables between the seagrassboundary and the interior parts of a patch or meadow, and/orthe unvegetated substrate (Table 2). However, some papersdiscuss ‘‘edge effects’’ based purely on comparisons betweenpatches of different sizes and perimeter: area ratios, thus ig-noring the possible effects of patch shape (Bell et al., 2001and references therein). Due to many interacting/co-varyingfactors at the patch level, the most studied local-scale variablewas structural complexity (62%) based on shoot density, mor-phology (leaf length, width, area) above and/or below-groundbiomass and/or seagrass species composition. Althoughpatches within seagrass landscapes are rarely symmetrical,but occur in a variety of shapes, our understanding of therole of patch shape, orientation and quality (food availability)for associated animals is still based on a very limited number(<10%) studies.

393C. Bostrom et al. / Estuarine, Coastal and Shelf Science 68 (2006) 383e403

In terms of landscape scale variables, about 50% of all stud-ies focused on some aspect of seagrass ecosystem configura-tion based on a variety of partly correlating metrics,including fragmentation, proximity, connectivity, isolation,fractal dimension, total linear edge, number of patches, edgecontrast and patch orientation (Table 2). At its simplest, frag-mentation is usually observed as a reduction in seagrass coverand a decrease in patch size over time, causing an increase inthe proportion of habitat edge and distance between patches,i.e. decreased connectivity and increased amount of unvege-tated corridors. However, the definition of habitat fragmenta-tion per se should be limited to the breaking apart of habitatafter controlling for habitat loss. Consequently, the effects ofhabitat fragmentation per se and loss should be measured in-dependently (for a review of these concepts, see Fahrig,2003). Although habitat fragmentation is a process, whereecosystems are divided into smaller pieces, in seagrass land-scape studies, fragmentation is seldom measured as a trendover time. Instead, the term fragmentation is mostly used fordescription of a static arrangement of patches, and althoughfragmentation is a landscape-scale process, its effects are usu-ally studied indirectly and at the patch scale. Although frag-mentation is characterised by the number and sizedistribution of the resulting patches, we found only a singlestudy reporting an estimate of number of patches per unitarea investigated (Salita et al., 2003), and no study assessedfaunal responses of patches undergoing fragmentation. In sum-mary, most studies have not addressed the actual process of

0

5

10

15

Num

ber

of s

tudi

es

0.5-10 10-50 50-100 100-200 200-500 500-3000

Patch size class (m2)

0

10

20

30

Num

ber

of s

tudi

es

0.1 1 10 100 1000 10000

Patch size (m2)

a

b

Fig. 2. Size distribution of seagrass patches reported in the examined literature

(1994e2004) presented as size classes (a) and minimum size (dot) and range

(line) (b).

fragmentation, but rather patterns which serve as surrogatesfor the results of fragmentation and habitat loss (but see Hea-ley and Hovel, 2004). Less than 20% of all studies reported es-timates of percent seagrass coverage, while empirical evidenceof the existence and ecological role of corridors (either vege-tated or unvegetated) is still limited to only a few (6%) exam-ples. Five studies considered other habitats (oyster reefs,macroalgae and saltmarshes) within the seagrass landscape.

3.3. Faunal response to landscape structure

The majority (>80%) of studies focused on invertebrates.Mollusca (almost exclusively bivalves) was the most studiedtaxon (34%), followed by epifaunal and infaunal assemblages(28% and 25%, respectively), crabs and fish (21% each), whileshrimps were included in 12% of the studies (Fig. 1b). Themost common response variables describing faunal populationand community structure in relation to patch and landscapevariables were density (>65%) and number of species/taxa(25%), followed by composition, biomass and diversity, eachcontributing by about 10% (Fig. 1c). These studies tended tocapture the broad-scale effect of landscape structure on faunalcommunity composition, but studies at different scales wererequired to address the role of landscape attributes in the func-tional performance of individuals or species. Functional pro-cesses studied included mortality/survival (34%), and growth(21%), while predation, movement and recruitment contrib-uted by 9, 9 and 6%, respectively (Fig. 1d). At the individuallevel, body size and condition were the most studied parame-ters, contributing by 15% and 6%, respectively (data notshown in Fig. 1).

The three most commonly studied explanatory variables,i.e. patch size (natural patches or ASUs), edge effects andfragmentation, and the five most commonly studied animal re-sponse variables, i.e. density, number of species/taxa, growth,predation and mortality, were chosen for closer examination.In two thirds of the studies examined, seagrass patch sizewas a significant predictor of density (n ¼ 7), growth (n ¼ 5)and mortality (n ¼ 4), respectively. However, half of the stud-ies examined showed non-significant results for the same re-sponse variables, mainly due to confounding effects of sites,seasons and target taxa. This exemplifies the difficulty in link-ing effects of seagrass landscape pattern to faunal structure.When patch size effects on animal densities were standardizedto overcome confounding effects, and tested using ASUs, theresults are contrasting, with the equal proportions of signifi-cant (Eggleston et al., 1998; Laurel et al., 2003) and non-significant (Bologna and Heck, 2000; Eggleston et al., 1999)results, respectively.

In >80% of the studies (n ¼ 11) of faunal responses topatch edges, a significant effect was found on organism den-sity, while non-significant edge effects on densities were re-corded in 40% of the studies. Growth responses to seagrasshabitat edges (n ¼ 2) were inconclusive, i.e. both significant(Bologna and Heck, 1999a; Reusch and Williams, 1999) andnon-significant (Reusch and Williams, 1999). In 75% of thestudies, fragmentation was a significant predictor of prey

394 C. Bostrom et al. / Estuarine, Coastal and Shelf Science 68 (2006) 383e403

density (Hovel and Lipcius, 2001; Hovel et al., 2002; Salitaet al., 2003), and predation rates (Irlandi, 1994; Irlandiet al., 1995). Measured as faunal mortality, fragmentation(patch size and configuration as explanatory variables) re-sulted in a similar number of significant (n ¼ 4) and non-sig-nificant (n ¼ 5) results. In over 60% of the studies, habitatcomplexity had a significant effect and co-varied with explan-atory patch and/or landscape variables (e.g. Irlandi, 1994;Turner et al., 1999; Hovel et al., 2002; Bologna and Heck,2002; Salita et al., 2003).

3.4. Taxon-specific responses to patch and landscapevariables

3.4.1. Patch size effectsVery few studies (n ¼ 2) examined species-area relation-

ships. Bowden et al. (2001) reported a positive relationship be-tween total number of macroinvertebrate taxa, (but notdiversity) and patch size, while Bell et al. (2001) reportedno significant effects of patch size on total number of amphi-pod species. Manipulative experiments with ASUs, haveshown no patch size effects on number of macroinvertebratespecies or density (Eggleston et al., 1999), while specifictaxa such as crabs and fish seem to respond positively to in-creasing patch size (Eggleston et al., 1998; Laurel et al.,2003), while shrimp densities have shown opposite or non-significant responses to patch size (Eggleston et al., 1998).

No clear patterns emerge when patch size effects weretested among the most studied faunal groups, i.e. peracarids,decapods, fish and bivalves. In total, 17 vs. 14 and 7 vs. 7 sig-nificant and non-significant results were reported for naturaland experimental (using ASUs) patch size studies, respectively(Fig. 3a,b). Patch-size effects on growth have only been stud-ied for bivalves. These studies (n ¼ 4) showed equal propor-tions of positive, negative and non-significant responses toincreasing patch size, but there was also evidence that covari-ation with structural complexity influenced the results (Irlandi,1996). In one study (Reusch and Williams, 1999) bivalvegrowth in terms of condition showed both a non-significantand a negative relationship with increasing patch size. Fivestudies focused on mortality. Two thirds of these studies fo-cused on crabs as prey and reported both positive and negativerelationships between crab mortality and patch size, and twonon-significant results. Bivalve mortality appeared to be sig-nificantly negatively correlated with patch size (Irlandi,1997; Irlandi et al., 1999) but non-significant results werealso reported (Irlandi et al., 1999).

3.4.2. FragmentationSeagrass habitat fragmentation effects on decapods, fish

and bivalves have been inconclusive, with about equal propor-tions of significant (56%) and non-significant (44%) results,respectively (Fig. 3c). In particular, density and mortality ofcrabs have been shown to correlate both positively (Hovelet al., 2002; Hovel and Lipcius, 2002) and negatively (Hoveland Lipcius, 2001), or show no significant correlation (mortal-ity) with increasing fragmentation (Hovel, 2003). Predation

rates (both sub-lethal and lethal) and subsequent mortality ofbivalves have mostly been shown to correlate positively withincreasing fragmentation. Examples of responses of fish densi-ties to fragmentation are few (n ¼ 2) and show both higher andlower densities in fragmented seagrass landscapes comparedto more continuous landscapes (Hovel et al., 2002; Salitaet al., 2003). Total number of species of fish and decapodshas been demonstrated to show a negative relationship withincreasing fragmentation, while non-significant patterns havebeen demonstrated for infaunal density, taxa richness anddiversity.

0

5

10

15

Non-significant (14)

Significant (17)

Seagrass patch size

0

5

10

15

ASU size

0

5

10

15

Peracarids Decapods Fish Bivalves

Edge effects

0

5

10

15

Fragmentation

n.d.n.d.

n.d.

n.d.n.d.

n.d. n.d.

n.d.

Non-significant (7)

Significant (7)

Non-significant (7)

Significant (9)

Non-significant (9)

Significant (22)

a

b

c

d

Fig. 3. Number of significant (P < 0.05) and non-significant effects of seagrass

patch size (a), ASU size (b), fragmentation (c) and edge effects (d) on

peracrids, decapods, fish and bivalves. Total number of significant and non-

significant results, respectively, are given within parentheses.

395C. Bostrom et al. / Estuarine, Coastal and Shelf Science 68 (2006) 383e403

3.4.3. Edge effectsPeracarids showed clear responses to habitat edges, with

>80% of all tests being significant. In all peracarid studies, an-imal densities were significantly higher along edges comparedto interior parts of a patch or meadow (Fig. 3d). Edge effectson bivalves and decapods have been less studied (4 and 4 stud-ies, respectively), and showed higher and/or equal densities ofbivalves along seagrass patch edges. Decapod studies haveshown either negative (density) or non-significant (density,size) responses to habitat edges. One study reported signifi-cantly lower densities of total macrofauna and fish along edges(Uhrin and Holmquist, 2003). Responses of infauna to habitatedges are less pronounced, but three studies (Bowden et al.,2001; Bologna and Heck, 2002; Tanner, 2004) have demon-strated higher polychaete densities along edges, but oppositedensity patterns and non-significant results have also beenshown for polychaetes (Bell et al., 2001). Reported functionalresponses to habitat edges are few, but shrimp and crab sur-vival times have been demonstrated to be lower at edges (Pe-terson et al., 2001). Higher growth rates but simultaneouslyhigher mortality of bivalves along seagrass edges have alsobeen reported (Bologna and Heck, 1999a).

3.5. Proposed mechanisms behind observed animalresponses

Seagrass landscape structure has specific effects on manyphysical and ecological processes. We explore only brieflythe mechanisms behind animal responses to patch size andedge effects, fragmentation and corridors. For a more detailedreview of explanatory models put forward, see Connolly andHindell (this issue). In general, we found that a landscape vari-able by itself seldom explained adequately the variance inresponse variables directly; rather they influenced faunaldistributions and dynamics indirectly, for example by alteringthe following:

(1) Water flow, physical disturbance and sediment character-istics. At high-energy sites seagrass patches containsmore fine sediment material than unvegetated sediments,while at low-energy sites there is no such difference(Irlandi, 1996). In particular, sediments from large patchesmay have higher percentage of fines (<63 mm) than smallpatches, which in turn influence infaunal assemblage com-position (Frost et al., 1999; Bowden et al., 2001). Horizon-tal water movement may also decrease with increasingpatch size, thus modifying food availability (particulatechlorophyll a) and growth of bivalves (Bologna andHeck, 1999a; Reusch and Williams, 1999). The hydrody-namic regime also largely determines larval supply rates.Reduction of water flow by seagrass may cause accumula-tion of recruits along seagrass edges (Bologna and Heck,2000), but size, shape and orientation of seagrass patchesmay also influence post-settlement distributions (Tanner,2003). Alterations of within-landscape hydrodynamicsby landscape configuration may also influence growthand/or structural characteristics of the seagrass, including

shoot density, morphology, above and below-ground bio-mass and seagrass species composition.

(2) Predation pressure. Seagrass spatial pattern, independentof plant density and biomass, may alter predation ratesand foraging strategies of nekton, e.g. scallop survival de-crease with decreasing seagrass cover (Irlandi et al., 1995).Specific landscape structures, such as vegetated (Micheliand Peterson, 1999) or unvegetated (Irlandi et al., 1995;Bell et al., 2002) corridors, also affect mobility of preda-tors. Corridors enable predators to remain near shelterwhile moving in search of prey. Such vegetation patternsmay alter predator distributions and increase predatoreprey encounter rates and foraging success along outeredges. Thus, scallops living along seagrass bed edges ex-perience higher predation pressure than scallops living ininterior parts or on unvegetated sediment (Bologna andHeck, 1999a).

(3) Movement and behaviour. Tag and release experimentshave demonstrated that bay scallops released on baresand actively move into seagrass and aggregate along sea-grass edges (Bologna and Heck, 1999a). Similarly, higherabundances of large decapods in continuous or largepatches of seagrass may be explained by active habitatchoice, i.e. an anti-predator behaviour response to avoidhigher order predation. Patterns of shrimp densities in re-lation to patch size have been suggested to be due to edgeeffects, but whether the mechanism is refuge or foraging isunclear (Eggleston et al., 1998). Examples of responses offish assemblages to differences in seagrass habitat config-uration are still rare, but is likely to involve trade-offs be-tween optimal foraging under predation hazard in a patchyenvironment, and less efficient foraging in continuous sea-grass while gaining protection from predation (Salita et al.,2003). The quality and proximity of the adjacent habitathave also been demonstrated to affect movement patternsand abundance of estuarine fish (Irlandi and Crawford,1997).

(4) Reproduction strategies. Life-history traits, includinghigher or lower fertilization success and reproductive out-put in edge habitats, have been put forward as explanatorymechanisms for (usually higher) faunal densities in sea-grass edge habitats (Bologna and Heck, 1999a, Bolognaand Heck, 2000; Bell et al., 2001; Brooks and Bell,2001). In addition, an organisms’ ability to colonize andcompete, and their body size and feeding mode has beensuggested to explain differences in faunal distribution infragmented seagrass landscapes (Bowden et al., 2001).

In addition to these pathways a number of covarying mech-anisms may explain both the landscape configurations andstructural complexity, but also directly influence the fauna,e.g. hydrodynamics and geology. We found that a landscapevariable, by itself seldom explained adequately the variancein response variables; rather, covarying mechanisms typicallyexplained faunal distributions and dynamics. Variables covary-ing with patch size were e.g. growth and/or structural charac-teristics of the seagrass, including shoot density, morphology,

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above and below-ground biomass and seagrass species compo-sition (Irlandi, 1997; Hovel and Lipcius, 2001). Also predatordistribution, hydrodynamics and accumulation of fines havebeen reported to covary with patch size (Bowden et al.,2001; Hovel, 2003). Covarying factors can be seagrass speciesspecific, and the relation may vary in both space, i.e. region-specific effects, and time, i.e. season-specific effects (Hoveland Lipcius, 2001). Also, landscape cover and specific ele-ments of landscape configuration typically covary. For exam-ple, patch area and nearest neighbour distances vary withpercent cover. Consequently, many landscape metrics are cor-related and provide redundant information (Ritters et al.,1995). Covariation makes it difficult to determine differencesbetween local and landscape phenomena, but can be statisti-cally removed to obtain independent measures (see Hovel,2003).

4. Discussion

4.1. Is fragmentation of seagrass habitats important?

Based upon the general principle that species diversity ishigher in seagrass compared with adjacent bare sand habitats(e.g., Arrivillaga and Baltz, 1999; Uhrin and Holmquist,2003, but see Hanekom and Baird, 1984; Jackson et al.,2002), loss of seagrass would result in a reduction of speciesdiversity. While no general distinction between habitat lossand habitat fragmentation per se is usually made (Fahrig,2003), the literature examined here, used the term fragmenta-tion to indicate decreased proximity, connectivity, and in-creased isolation. Fragmentation has generally been broadlyapplied as a synthetic term for all aspects of ecosystem changeincluding spatial configuration of patches (Forman, 1995;Bender et al., 1998; Rutledge, 2003). In the seagrass landscapepapers dealing with planteanimal interactions examined here,fragmentation was not measured as a process over time, butmostly used for description of a static arrangement of patches.Such approaches only provide clues of possible responses tohabitat fragmentation. While temporal dynamics of seagrasslandscape mosaics have been extensively documented (e.g.Kendrick et al., 1999; Robbins and Bell, 2000; Frederiksenet al., 2004 and references therein), we are unaware of studiessimultaneously monitoring possible faunal responses to sea-grass fragmentation.

We found mixed effects of fragmentation in seagrass land-scapes, with about equal proportions of significant (both pos-itive and negative effects, see above) and non-significanteffects, respectively, suggesting that seagrass fragmentationis not necessarily detrimental for associated animals. Thismight be the case if fragmentation of seagrass does not resultin its replacement by unvegetated substrate. For example, sea-grass fragmentation can be the result of invasive macroalgae(Villele de and Verlaque, 1995) or the addition of an anthropo-genic structure both of which are structural habitats that mayconvey some benefits to certain fauna (Heck et al., 2003).However, several other mechanisms acting in the marine envi-ronment may also be responsible for this result.

In terrestrial settings, landscape fragmentation is consid-ered to be one of the most important factors leading to lossof biological diversity (Hanski and Gilpin, 1997). In seagrasslandscape studies, faunal diversity per se and community ecol-ogy in general, has received little attention. Rather, much ofour present understanding of landscape fragmentation effectsis based on a few single-species case studies, i.e., crab, shrimpand bivalve responses. Studies in terrestrial landscapes havedemonstrated critical thresholds in fragmentation, where mo-bility and diversity patterns change dramatically and non-linearly (Gardner and Milne, 1987; Rosen, 1989). In seagrasslandscapes, thresholds in cover area have been related to phys-ical setting, and Fonseca and Bell (1998) suggested possiblefunctional changes/effects on associated organisms when cov-erage drops below the 59% level. Demonstration of suchthreshold responses of organisms warrants further investiga-tion in different environmental settings and geographicallocations.

Broad-scale movement of marine invertebrates occurs pre-dominantly by means of passive dispersal of larval reproduc-tive stages, eggs and juveniles over vast areas, compared toactive movement by adults or sub-adults in the terrestrial land-scape. This implicates the important role of increased connec-tivity between marine populations compared to terrestrialcounterparts, and possibly a minor role of corridors in the ma-rine environment. Thus, in contrast to terrestrial landscapeswhere reduced connectedness lowers population recruitment,the increased total amount of edge in patchy seagrass habitatsincreases encounter rates of larvae and animals that are depen-dent on physical transport mechanisms (Bologna and Heck,2000). Accordingly, McNeill and Fairweather (1993) recordedmore macroinvertebrates and fish in several small patches ofthe same combined area as a single large, and explained thispattern by increased probability of interception due to in-creased perimeter: area ratios of smaller patches, and/or dueto increased likelihood of sampling edge habitats in smallerhabitats.

In accordance with terrestrial studies suggesting minor ef-fects of fragmentation on migratory and edge species (Benderet al., 1998), studies of actively moving crustaceans indicatethat fragmented seagrass supports more decapods than doescontinuous seagrass (Eggleston et al., 1998; Loneragan et al.,1998; Hovel and Lipcius, 2001). Eggleston et al. (1998) foundhigher densities of grass shrimp at small seagrass patch sizes,and Loneragan et al. (1998) found lower numbers of juvenilefish and prawns with increasing seagrass cover. However, al-though small patches may support high densities of organisms,this does not necessarily translate into higher total densitiesof organisms in a fragmented seagrass landscape comparedto a continuous landscape. One of the arguments for greaterprawn and crab densities in fragmented seagrass landscapesis that predator efficiency is lower in fragmented seagrasslandscapes. This is because the search for appropriate feedingpatches takes longer in fragmented seagrass (Hovel and Lip-cius, 2001). Predators may also avoid moving into fragmentedareas of a landscape due to their potential vulnerability, or dif-ferences in the density of their prey organisms (Micheli and

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Peterson, 1999; Hovel and Lipcius, 2001). Conversely, otherspropose that patchiness facilitates foraging (Irlandi, 1994), andmay lead to a higher proportion of active foraging speciesfound in patchy landscapes.

Patchy seagrass landscapes provide a more diverse habitat,particularly if the seagrass landscape is a mosaic of sand, sea-grass and algal habitats. This would attract nekton with bothpreferences for vegetation and bare substrata, which followsLeopold (1933) theory of increased habitat diversity leadingto increased faunal diversity. For example, Salita et al.(2003) found high numbers of large benthic feeding fish invery fragmented seagrass habitats, but these were replacedby high numbers of small, juvenile or cryptic species inmore continuous seagrass landscapes. Thus, in accordancewith Turner et al. (2001), it might be summarized that effectsof spatial patterns/fragmentation on organisms are not likely tobe important if habitat patches are abundant (in terrestrial en-vironments >30% cover) and well connected, edge effects arenot central to the process/species under study, and movementbetween suitable habitats is relatively unlimited.

4.2. Can models be generalized across landscapes?

In this review, landscape variables were seldom significantpredictors of invertebrate response variables. Rather, patchscale and landscape scale variables interacted and covariedin 60% of the studies, with usually strong effects of within-patch plant characteristics on animal responses. Consequently,the influence of the seagrass landscape scale on ecosystemfunction only occasionally appears to override local scale var-iability. The literature surveyed suggests also that seagrasslandscapes support highly dynamic communities where resultswere seldom consistent over time within the same region(Irlandi et al., 1999; Bologna and Heck, 2000, 2002; Bellet al., 2001; Hovel and Lipcius, 2001; Salita et al., 2003) oracross sites (Irlandi, 1996; Hovel et al., 2002; Egglestonet al., 1999).

Accordingly, in a review of terrestrial studies examiningboth patch (area, structural characteristics, composition, orien-tation, shape) and landscape (configuration and cover) vari-ables, landscape variables predicted species presence anddensity in only 7% of the studies, but were significant inhalf of the studies when combined with patch variables(Mazzerolle and Villard, 1999). In particular, invertebratesappeared less sensitive to landscape variables than vertebrates,with less than 12% of the studies of invertebrate responsesreporting significant effects of habitat configuration, and nostudy reporting a significant effect of cover.

The island biogeographic model, which describes seagrasspatches as a focal patch in a matrix of a ‘‘hostile’’ alternativehabitat, is often criticised because it is unlikely that organismsexhibit a binary response to patch types such as seagrass, butinstead use the landscapes proportional to the fitness they con-fer to the organism (McGarigal and Cushman, 2002). Thusmany of the studies discussed and the models for survivaland faunal distributions cannot be generalized across land-scapes or across species (responders). An alternative to the

island biogeographic view, therefore, is that seagrass land-scapes are a complex mosaic of habitats, where distinctionsbetween elements more or less similar to focal patches are de-pendent on the perspective of the organism or process beingstudied or the specific management question.

Since landscape ecology in seagrass ecosystems has notbeen applied as broadly as in terrestrial systems, we are per-haps not yet at a comparable level, and thus lack sufficient in-formation to suggest that a fluid media makes a significantdifference compared to terrestrial ecosystems. However, dueto the many differences between marine and terrestrial ecosys-tems, the validity of transferring landscape ecology principlesfrom our terrestrial experiences to estuarine and marine eco-systems may be suspect (Fairweather and McNeill, 1993;McNeill and Fairweather, 1993).

Seagrass landscape studies are generally conducted ata much smaller scale compared to terrestrial counterparts,where patch sizes typically exceed thousands of hectares(Mazzerolle and Villard, 1999). Seagrasses also representmuch simpler systems in terms of height and structural com-plexity of the canopy elements compared to terrestrial vegeta-tion (Robbins and Bell, 1994). However, a seagrass landscapemay be classed as homogenous in terms of being completelycomposed of seagrass, whilst actually being a mosaic of struc-turally different seagrass species patches. The limited geo-graphical distribution of seagrass landscape studies (75% ofall studies conducted between 30 � N and 40 � N) in our reviewlimits generalizations regarding the importance of diversity oflandscape components. In particular, the lack of comparativestudies between the architecturally simple and low diverse(1e3 seagrass species) temperate seagrass landscapes studiedto date, and tropical seagrass landscapes with assemblagescontaining >10 co-occurring seagrass species, have not al-lowed parallel comparisons with the terrestrial pattern of in-creasing density and diversity of animals in architecturallycomplex landscapes (Denno and Roderick, 1991 and refer-ences therein). Given the strong relationship that we noted be-tween structural characteristics and many invertebrateresponse variables, such comparisons beyond the temperateseagrass ecosystems would provide further insight to the im-portance of patch vs. landscape variables for ecological patternsand processes across latitudinal gradients (Virnstein et al.,1984; Heck and Wilson, 1987; Bostrom and Mattila, 1999,2005). A comparative approach could also uncover confound-ing influences of mixed vs. monotypic vegetation assemblages.

Other fundamental differences between terrestrial andmarine landscapes include minor importance of parasitism andseasonality (winter) which have been identified as chief mech-anisms causing population declines and extinction in small ter-restrial patches, lack of host specificity in seagrass landscapescompared to species-specific patch associations in terrestrialpatches, and a general lack of historical (19the20th century)distributional data in terms of aerial photographs of seagrasslandscapes. An additional difference is that in terrestrial sys-tems landscape configuration is often the result of anthropo-genic processes, while in seagrass systems these effects arecaused by natural processes (see Section 1).

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4.3. Faunal mobility and landscape perception

While movement behaviour has a key position within sev-eral disciplines of terrestrial ecology, (Hansson et al., 1995,and references therein), there is a paucity of solid empiricalinformation on space use by marine invertebrates (but seeEggleston et al., 1998; Holmquist, 1998). Critical questionsregarding how mobile seagrass fauna perceives and respondsto patchiness have only recently started to be explored. Thesmallest scales at which an organism responds to heterogene-ity (‘‘grain’’) is where it no longer perceives its environment ashomogenous, while the largest scales at which an organismresponds to patchiness (‘‘extent’’) is determined by the home-range during its entire life cycle (Kotilar and Wiens, 1990;Eggleston et al., 1998; Hovel and Lipcius, 2001; Attrillet al., 2000). Consequently, these measures are species-specificand while a landscape might appear fragmented to one speciesit could be perceived as continuous by another.

Patchy seagrass landscapes represent good model systemsto test which internal and/or external factors influence thesearching behaviour of organisms. Examples of attempts toquantify the degree to which seagrass patches are ‘‘open’’ or‘‘closed’’ are few (Holmquist, 1998), but the role of food re-sources in terms of epiphytes for animal immigration/emigra-tion ratios have been demonstrated for herbivore and omnivoretaxa (Bologna and Heck, 1999b).

The importance of unvegetated strips as corridors for largemobile predators (e.g., Irlandi et al., 1995) is likely to vary de-pending on target species and water depth. In very shallowseagrass landscapes, where the leaf canopy reach the watersurface, unvegetated corridors may provide the only avenuefor movement/foraging in an unstructured environment, whilein deeper seagrass landscapes the space above the leaf canopycan also be utilized by mobile fauna. Bell et al. (2002) foundthat pinfish (Lagodon rhomboides) utilised propeller scarringin a Thalassia testudinum landscape as corridors. Similarly,Holt et al. (1983) found red drum (Sciaenops ocellatus) tobe more abundant in patchy areas than in homogenous standsof Halodule wrightii and suggested that this greater abundancewas related to the juvenile fishes’ requirements for open feed-ing areas adjacent to seagrass that provided nearby protectionfrom larger predators. Drifting algae are common featureswithin seagrass mosaics (Bell et al., 1995) and can provideprotection during dispersal among patches. Drifting algaehas been shown to facilitate shrimp and amphipod movement(Holmquist, 1998; Brooks and Bell, 2001). Although terres-trial evidence suggest that species tolerating edges are alsolikely to utilize corridors (Lidicker, 1999), there is still littleexperimental evidence of the role of corridors (unvegetatedor vegetated) for animal movement patterns in seagrasslandscapes.

More experimental work is also needed to predict whichpatch attributes (shape, quality, structural complexity) becomeimportant to maintain ecosystem function as the total area de-creases. Knowledge regarding space use and perception ofpatchiness by animals dependent on seagrass is not only crit-ical for experimental design issues (e.g., ASU size and

spacing) but also for restoration efforts (see below). Presently,the size range of ASUs are limited by logistical reasons, andseldom based on home-range or perception information ofthe organism under investigation.

4.4. Infaunal response to landscape structure

The responses of infaunal assemblages to landscape struc-ture have received considerably less attention compared to epi-faunal studies and species-specific (mostly bivalve) studies.Surprisingly, given their inability to rapidly adjust to predationand other dynamic influences in seagrass landscapes, infaunalassemblages showed usually weak responses to landscape var-iables, leaving much of the variability unexplained (Tanner,2003; Bowden et al., 2001; but see Turner et al., 1999). Infau-nal communities are suggested to be least affected by frag-mentation compared to large motile fauna, and showspecies-specific effects and/or small shifts in community com-position rather than dramatic changes in density (Frost et al.,1999). In general, infaunal assemblages appear to be primarilycontrolled by sediment stability and grain size, which both co-vary with shoot density, below-ground biomass and the phys-ical setting of the landscape mosaic (Bostrom and Bonsdorff,1997, 2000; Bowden et al., 2001). The generality of infaunalcommunity responses to seagrass landscape pattern awaits fur-ther investigation.

4.5. Implications for seagrass management andrestoration/conservation

Although terrestrial landscape ecology has a long history ofapplication to conservation and management, particularly inthe case of locating and designing reserves and in managingresources to minimize or restore at-risk fish and wildlife pop-ulations (e.g., Hansson et al., 1995; With and Crist, 1995; Withet al., 1997), seagrass landscape structure is not often ad-dressed in coastal zone management and restoration. Thevalue of seagrass and of areal extent is certainly recognizedas a desirable factor to be managed as ‘‘critical nursery habi-tat’’ of fisheries resources, although validation of the causativefactors or seagrass landscape attributes that actually accountfor enhanced survival to recruitment is lacking (Beck et al.,2001). In contrast to previous assumptions, it has been demon-strated that many taxa have limited larval dispersal abilities,implying that such fauna will respond negatively to increasingfragmentation, and that maintenance of connectivity amonghabitat patches is indeed an important management issue(Ruckelshaus and Hays, 1998). Linkages of seagrass habitatsof nekton to other adjacent habitats, such as saltmarshes andmangrove forests, have also been addressed in several cases(e.g., Irlandi and Crawford, 1997; Micheli and Peterson,1999), suggesting synergistic effects at the landscape level,and conservation of mosaics of sites rather than single sites.But, with a few exceptions, (e.g., McNeill and Fairweather,1993; Fonseca et al., 1990), seagrass restoration has tendedto focus almost entirely on persistence and spatial extent ofplanted or recruited plants and various metrics of overall

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seagrass quality, such as shoot density and above-ground bio-mass rather than metrics of the seagrass landscape structure.The fact that no phenomenon is separate from a landscapecontext (Allen and Hoekstra, 1992) would seem irrefutablein the case of the complex landscapes that seagrasses formand reside within. Yet, specific attributes of seagrass land-scapes that sustain organisms through population and ecolog-ical phenomena are poorly known, at least not to the point thatthey have been implemented in management and restoration.

Naveh (1994) and Bell et al. (1997, 2001) have particularlypromoted the extension of our emerging understanding of fau-nal responses to seagrass landscapes to conservation biologyand restoration ecology. The influence of the spatial arrange-ment of landscape elements on metapopulation dynamicsand population processes such as migration was one of fivemajor research needs identified by Montalvo et al. (1997) asunique opportunities to couple basic research with the practi-cal needs of restoration. However, despite the fervent argu-ments for the applicability, landscape concepts have yet tobe translated into rigorous restoration experiments. Themany seagrass transplanting and monitoring opportunities inrestoration actions remain comparatively unexploited for test-ing the faunal responses that are typically the justification forthe restoration.

4.6. Gaps in knowledge and future directions

� To test the generality of landscape effects observed, thelimited geographical distribution of seagrass landscapestudies needs to be significantly extended to encompassdifferent biogeographic regions including both Europe aswell as tropical and cold temperate regions.� More information is needed of seagrass landscapes with

high structural and seagrass species diversity, patterns andmechanisms of subtidal (>2 m deep) seagrass landscapes,and studies addressing faunal community- or ecosystem-level performance variation with landscape structure.� Since the predation model has been the most frequently

put forward model to explain faunal response variablesin seagrass landscapes (Fig. 1d and Connolly and Hindell,this issue), more contrasting studies are needed betweenanimals in seagrass landscapes experiencing high vs. lowpredation pressure. Such an approach could demonstratepossible co-evolution of predators and prey in differentlandscape configurations.� Most of the faunal research has focused on vegetated

patches, while there is a paucity of information regardingthe importance of the matrix habitat, i.e., faunal patterns inunvegetated patches embedded within the seagrass.� Compared to terrestrial studies, seagrass landscape studies

are still conducted at small scales. Existing spatial modelsneeds to be tested at various scales, in particular field val-idation of scaling up results from fine-scale experiments tolandscape scales. Other than a few studies linking seagrassecosystems to other habitats (mangroves, saltmarshes,reefs) there are few studies that provide the landscape con-text per se.

� Patchiness needs to be defined relative to the species underinvestigation. Modelling relationships at different scalesshould reflect the perceptions of the organisms under study(perception of edge and also their natural ranges). This re-quires good understanding of the species biology andwould allow for decisions about correct scale and/or dem-onstration of cascades. This is particularly the case withreal time movement of organisms through seagrasslandscapes.� Use ASUs to simulate metrics which cover combinations

of the different aspects of a patch, not just size, shapeand edge. There is also a need to conduct other manipula-tions of natural seagrass patches to reflect not onlychanges in landscape metrics, but other internal (epiphyteload, seagrass species composition) and broader-scale at-tributes such as current regimes, freshwater inflow anddepth differences.� Although partly beyond the scope of this paper, relatively

little is still known about plant responses to landscape pat-terns. These include reproduction responses (flowering andseed dispersal), genetic attributes, spatial patterns of epi-phytes and performance and growth of plants at differentpositions within the landscape.

5. Conclusions

The spatial patterns of seagrass landscapes have been rec-ognized as an important part of many processes, but are notthe singular causes dictating faunal patterns. Consequently,apart from ASU studies, many of the field studies to dateare confounded by factors that affect landscape configurationand directly the fauna, e.g. seagrass autecological factors, nat-ural and anthropogenic disturbance, depth and exposure. Non-linear relationships between ensemble faunal variables andlandscape metrics were identified by a number of studies,and are to be expected when assessing species with differentperception of the seagrass landscape. This may also accountfor the lack of relationships in some studies and the opposingresults of comparable studies. Relationships between a seagrasslandscape and/or plant characteristics and mobile fauna are of-ten species specific due to factors such as the size, behaviour,mobility and the dispersal ability of the organism and its per-ception of patchiness. In order to contrast patterns across re-gions and to allow the synergistic development of ourknowledge in this field, we need to standardise our use of land-scape metric and terms in relation to seagrass landscapes. Per-haps the more daunting need is a much better understanding ofthe various processes operating at various scales and possiblecascading effects across scales that influence fauna-environ-ment relationships in seagrass landscapes. It is obvious fromthis literature that they are complex, difficult to predict andstill relatively under-studied.

Acknowledgements

We are very indebted to the organizers of the ECSA37-ERF2004 meeting in Ballina, New South Wales, Australia,

400 C. Bostrom et al. / Estuarine, Coastal and Shelf Science 68 (2006) 383e403

20e25 June 2004, for the opportunity to organize a specialsession that drew the authors, and the affiliated authors repre-sented in the other papers in this volume, together. In particu-lar, we thank Brad Eyre and the Conference Secretary, forfacilitating such an effective meeting. We would like to ac-knowledge those presenting and present at the Seagrass Land-scape Ecology Session for the valuable discussion of some ofthe issues raised in this paper. We also thank Rod Connolly,Griffith University, who so willingly reoriented preparationand timing of his review (Connolly and Hindell, this issue)to fit this session synthesis. Kevin O’Brien commented on ear-lier drafts of the manuscript. C.B. was funded through a post-doctoral research position provided by the Academy ofFinland. Abo Akademi University and Svenska Kulturfondenare acknowledged for financial support to C.B. to attend inthe ECSA37-ERF 2004 meeting. E.L.J. would like toacknowledge the European Union 6th Framework programme,European Lifestyles and Marine Ecosystems (ELME), forfunding her postdoctoral research position and contributingto the travel for attending the ERF/ECSA meeting. C. A. S.was funded in part by a contract with the Point-No-PointTreaty Council and the Washington Sea Grant Program.

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