facilitation in mangrove ecosystems - aces · mangrove trees. we begin with the initial...

Cambridge University Press978-1-108-41608-5 — Interactions in the Marine BenthosEdited by Stephen J. Hawkins , Katrin Bohn , Louise B. Firth , Gray A. Williams More Information

www.cambridge.org© Cambridge University Press

Chapter 17

Kropotkin’s Garden

Facilitation in Mangrove Ecosystems

Mark Huxham, Uta Berger, Martin W. Skovand Wayne P. Sousa

That is the watchword that comes tous from the bush, the forest, the river,the ocean – therefore combine,practice mutual aid.

Peter Kropotkin, Mutual Aid 1906

17.1 Introduction

Ecologists have studied ‘mutual aid’ (or facilita-tion) since at least the time of Kropotkin(1842–1921). But the ‘watchword’ which heheard with such force has not always beenheeded, remains poorly understood and is ratherloosely defined. A seminal early use comes fromConnell and Slatyer (1977), where building on thework of Clements (1916), they used ‘facilitation’to describe a model of community succession inwhich pioneer species modify the habitatallowing the colonisation of later ones. While thissuccessional implication remains common in theliterature, the word is also applied more broadlyto positive interactions between individuals andspecies. Some authors restrict the term to plant–plant interactions (e.g., Krebs, 2001), while otherstreat it as synonymous with ‘positive species rela-tionships’ (He et al., 2013), although Munguiaet al. (2009) argue that any relationship that does

not cause evolutionary changes to both parties isnot a true ‘interaction’. Others expand the termto describe any positive relationships betweenindividuals. For example Schöb et al. (2014) statethat facilitation describes ‘the positive effects ofone organism on others’, while Singer (2016)defines it as ‘interactions between two organ-isms, or two species, that benefit at least one ofthem and harm neither’. The latter definitioncovers interactions at all levels of complexity,from individual behaviour through to ecosys-tems, and includes obligate symbiosis, commens-alism and looser associations.

The term therefore always involves the idea ofbenefit from association with another organism.This benefit is sometimes mutual, sometimesone-way and sometimes even negative for onepartner, particularly over time (the facilitationmodel of succession allows for the competitiveexclusion of the pioneer species by those thatthey facilitate). Given this broad use, any reviewof facilitation is in danger of losing focus orbecoming overwhelmed. Here, we adopt anotherinfluential definition from Bertness and Calloway(1994), which includes interactions within andbetween species, but restricts the ambit of theterm through a focus on stress: ‘the benefits toan organism by the minimisation by neighbour-ing organisms of biotic or physical stress’. Appli-cations of this definition in the literature have

Mark Huxham, School of Applied Sciences, Edinburgh Napier University

www.cambridge.org/9781108416085

www.cambridge.org



emphasised facilitation through the ameliorationof physical stresses by habitat modification, bio-logical stresses through associational defencesand the existence of scale-dependant ‘positivehabitat switches’ (Wilson and Agnew, 1992), inwhich sufficiently large or dense associations oforganisms permit the presence of others. Here,we consider examples of all of these mechanismsin mangroves. We look at how relationshipsbetween individual plants can ameliorate phys-ical and chemical stresses (particularly duringestablishment and colonisation), and how theseeffects can manifest at ecosystem scales. We con-sider how fauna are known to change the phys-ical and chemical environments in favour of treeestablishment and growth, and how the bio-logical stress of herbivory may be mitigated byassociational defences conferred by spatial aggre-gation of plants or through indirect interactionswith epibionts or predators that defend plantsagainst herbivory. Finally, we discuss the possiblefunction of ecosystem-scale facilitation in thelong-term resilience of mangroves to environ-mental change.

17.2 Why Mangroves?

There are theoretical and practical reasons tolook for facilitation within mangrove ecosystems.The dominant conceptual model used to explainand predict the occurrence of positive inter-actions in ecosystems is the stress gradienthypothesis (SGH; Bertness and Callaway, 1994).This suggests that physical and biological stresseswill increase the frequency of facilitation, whichwill help mitigate these stresses through habitatamelioration or associational defences respect-ively. Later refinements of the theory show thatparticular outcomes of any interaction depend onthe characteristics of the stress factors (resourcesor non-resources) and on the performance of theinvolved species (relative stress tolerance andcompetitiveness), which might change duringtheir life cycles (Maestre et al., 2009).

Intertidal habitats are often used to exemplifystress in the ecological literature; they are placessubjected to frequent physical and chemical

changes and require adaptations suited for aqua-tic and terrestrial survival. So it is not surprisingthat many of the studies demonstrating facilita-tion and testing the SGH have been conducted inthe intertidal, with rocky shores and salt-marshhabitats predominating (see references in He andBertness, 2014). Mangroves are exposed to thesame stresses but are poorly represented inthe facilitation literature. Trees and shrubs arethe plant forms most likely to show strong facili-tative interactions (He et al., 2013) so those grow-ing intertidally – mangroves – should beparticularly likely to demonstrate them. Facilita-tive interactions may also help explain the highproductivity of mangrove ecosystems. Many ofthe adaptations to stress exhibited by mangroves,such as investment in succulent leaves with thickepidermal layers, metabolically costly salt exclu-sion, high root:shoot ratios and conservativeresource capture and growth strategies, are usu-ally associated with relatively low productivity(Chapin et al., 1993). The fact that mangrovesshow total productivity levels similar to terres-trial tropical forests (Alongi, 2009), despite theseadaptive characteristics, suggests we lack a fullunderstanding of how productivity is achieved inmangroves.

A growing literature indicates that fauna helpexplain this anomaly. The abundant burrows andmounds visible in most mangrove forests showecosystem engineers – particularly crabs – atwork. The activities of large and active bioturba-tors in areas where the edaphic conditions arestressful to plants creates conditions in whichanimals are likely to make important changes togrowing conditions. While crabs are the focus ofmost of the relevant literature, there is good evi-dence of facilitatory importance to forest func-tioning of other faunal groups, including ants,birds and sponges. Here we review some of thatevidence, with emphasis on the facilitatory rolesof fauna in the establishment and productivity ofmangrove trees.

Large-scale mangrove destruction combinedwith a growing awareness of the importance ofmangroves for people and wildlife have led toglobal reforestation and restoration efforts.When modelled on silvicultural practicesdeveloped for terrestrial forests under benign

432 MARK HUXHAM, UTA BERGER, MARTIN W. SKOV AND WAYNE P. SOUSA



www.cambridge.org



environmental conditions, these efforts are oftenunsuccessful (Kodikara et al., 2017). Whileplanting seedlings in straight rows with large,even distances between them might minimizetimber loss through density dependent mortality(self-thinning) once the vegetation is closed,growing evidence shows enhanced risk of mortal-ity and reduced growth of single plants withoutneighbours. Facilitation theory and informationon the importance of fauna provides a perspec-tive that may inform restoration and rehabilita-tion of mangrove habitat (Gedan and Silliman,2009), particularly in harsh and degraded settingsand where positive biotic influences have beenoverlooked. This chapter considers the evidencefor facilitation, as defined by Bertness and Call-away (1994), at the different successional stagesof a mangrove forest and life stages of individualmangrove trees. We begin with the initial estab-lishment and growth of seeds and propagules(while colonising new areas and within estab-lished forests), consider the growth of seedlings,saplings and young trees, and consider the posi-tive role of biotic interactions in enhancing thelong-term persistence of the mangrove ecosystemin the face of environmental change.

17.3 Establishment andColonisation

17.3.1 Hydrodynamics at theSeaward Edge

Mangrove seedlings and propagules are particu-larly vulnerable stages and early growth andestablishment is often prevented due to physicaland biological stresses. For example, Balke et al.(2011) identify ‘windows of opportunity’ duringwhich mangroves may establish on tidal flats.These are periods during which hydrodynamicforcing is low enough to allow the initial growthof the plants; without such periods, seedlings arewashed away. Because the critical drag force ofwater required to dislodge a new seedlingincreases exponentially with the maximum rootlength (Balke et al., 2011), the very early daysduring which roots are small are the most vulner-able. Hence, the physical impacts of waves and

fast-moving water are critical stresses at the sea-ward mangrove fringe and on open tidal flats.Hydrological stresses limit establishment of newplants beyond current vegetated areas. The plantsthemselves modify these stresses by slowingwater down, reducing wave heights, stabilisingsediments against erosion with their roots andby encouraging sediment accretion and deposit-ing organic material into the sediment. This gen-erates biogeomorphic feedbacks that can lead toalternative states (open mud flat versus denseforest) with very sharp and rapid transitions(both spatially and temporally) between them(Figure 17.1).

Mangroves are effective in attenuating theenergy of waves; for example, Kandelia candel treesof only five to six years old reduced wave energyby 20 per cent over 100 m (Mazda et al., 1997),while Barbier et al. (2008) show reductions of upto 60 per cent over 100 m of Sonneratia caseolaris.

Some mangroves, such as Rhizophora mucronata,are incapable of establishment without shelteredconditions (Thampanya et al., 2002). In manysites, such species effectively rely on the protec-tion from waves and water movement providedby the seaward forest, consisting of pioneerspecies such as Avicennia marina and Sonneratia

alba to establish and regenerate. This differentialsusceptibility to wave impact and biogeomorphicfeedbacks between tree density and water move-ment provides one explanation for species zon-ation within mangrove forests and is an exampleof an ecosystem-wide facilitation effect.

Researchers have long discussed whethermangroves can act as active ‘land builders’ orwhether they simply passively follow new accre-tion (see for example the discussion on p. 106 ofSmith (1992) citing examples more than 120 yearsold). While elements of this debate continue(Alongi, 2008), there is now compelling evidencethat mangroves enhance sediment accretion,enable forest surface elevation and reduce ero-sion (Winterwerp et al., 2005; Mcivor et al.,2012; Krauss et al., 2014; Huxham et al., 2015).Measuring the changes in coastlines over timehas shown how mangrove removal can enhancerates of erosion, while forest preservation canreduce erosion and cause land progradation(Thampanya et al., 2006). Hence, mangrove

KROPOTKIN’S GARDEN: FACILITATION IN MANGROVE ECOSYSTEMS 433



www.cambridge.org



ecosystems help create stable conditions for theirpersistence and, in some cases, expansion,through the facilitative effects of tree density onwater and sediment dynamics.

17.3.2 Desiccation at the Landward EdgeAt Gazi Bay, southern Kenya, there are manyhectares of bare sediment between the landwardfringe of the natural mangrove forest and theterrestrial vegetation. These forlorn areas arestudded with the stumps of long-dead mangrovetrees, testament to an historical transition fromforest to bare ground. Local sources suggest thiswas caused by commercial extraction of wood atleast forty years ago (Kirui et al., 2008). Hence,the loss of trees caused an enduring change fromforest cover to a new ecosystem, characterised bybare ground and very low biodiversity. This sharptransition between two states is similar to thatfound at the seaward mangrove fringe and

suggests strong feedback processes are operating;in this case, driven not by water energy, but bysalinisation and desiccation (Figure 17.2). Canopyremoval exposes the sediment to the sun andallows rapid evaporation of pooling saline water.At Gazi this has resulted in salinisation (withsediment pore water at 89 PSU or more), prevent-ing seedling establishment and leaving ‘salty bar-rens’which are hostile to the growth of all higherplants. Under such conditions, forest recoverymay follow the opening of natural ‘windows ofopportunity’, such as unusually heavy rainfallevents coinciding with periods of seed or propa-gule production. The lengthy persistence of theGazi salty barrens suggests that no such windowshave opened here over at least the past forty yearsand active restoration involving the planting-outof seedlings was required to restore mangrovecoverage. New seedlings and propagules are veryvulnerable to desiccation. However Avicennia

Fig. 17.1 Biogeomorphic feedbacks between hydrodynamic stresses (including wave height and current speed) and the

impacts of mangroves on water movement help to determine the sharp transition zone between the mangrove forest and

open shore.




www.cambridge.org



marina is exceptionally tolerant of salt (Jayatissaet al., 2008), and seedlings older than three tofour months were able to survive and grow (Kiruiet al., 2008). Avicennia marina subsequently actedas a nurse species at this site, allowing the estab-lishment of wild seedlings of other mangrovespecies under the protection of shade and withenhanced sediment moisture and reduced salin-ity, an example of inter-specific facilitation (Hux-ham et al., 2010).

Similar interactions have been reportedbetween salt marsh vegetation and the blackmangrove Avicennia germinans, which showsenhanced survival and growth when associatedwith salt-marsh vegetation under high-stressconditions in the USA (Guo et al., 2013). Inthe Caribbean, forbs and grasses can also act asnurse species for mangroves, both through

ameliorating soil conditions and by physicallytrapping and supporting propagules (McKeeet al., 2007b).

Intra-specific facilitation is also commonduring the early growth stages of intertidalplants, including mangroves, and such inter-actions can be harnessed to enhance restoration(Gedan and Silliman, 2009). For example, Silli-man et al. (2015) showed increased biomass oftidal marsh grass Spartina sp. when planted inclumped rather than dispersed configurations attemperate sites. This effect was largely due to theamelioration of soil anoxia, with high densities ofplants sharing oxygen leaked from roots. Similarmechanisms, along with mutual shading, mayexplain why high-density clumps of Avicennia

marina seedlings showed enhanced survival inKenya (Huxham et al., 2010).

Fig. 17.2 Canopy removal at the landward fringe can result in salinisation, as salt water evaporates without the protection of

shade. This may establish a stable state characterised by hysteresis; rapid transitions and non-linear processes mean that it is difficult

to reverse the condition of the ecosystem. Here, planting of high-density Avicennia marina seedlings allows mangrove recovery

through intra- and inter-specific facilitation, as the seedlings cast shade, enhance soil organic matter and permit colonisation of other

species.




www.cambridge.org



17.3.3 Degradation Due to Changes inHydrodynamics and the Role ofPhenotypic Plasticity in EcologicalRecovery

Regular flooding is essential for the normal func-tioning of most mangrove ecosystems; physicalchanges that prevent this usually result in theloss or degradation of forests. For example, therewas rapid dieback after the construction of a roadcutting through the Ajuruteua Peninsula, north-ern Brazil, in 1974. The road, constructed parallelto the watershed, blocked inundation by tidalchannels and led to desiccation and a lethal accu-mulation of salt of the sediment. The erosion ofthe uppermost soil layer by wind contributed to aregime shift from a tall mangrove forest (with amaximum canopy height of 30 m; Mehlig et al.,2010) to a bare, hypersaline ground, similar tothe salty barrens of Gazi. This lasted almost thirtyyears before A. germinans seedlings were able torecolonize the area (Vogt et al., 2014), presum-ably during a natural window of opportunity. Thecolonisers developed as shrubs and thus adaptedto the salinity-induced osmotic constraints andwater scarcity (Peters et al., 2014). As nurseplants, the shrubs facilitated the survival andgrowth of con-specific followers (Vogt et al.,2014; Pranchai, 2015), which eventually switchedback to tree architecture (Vogt et al., 2014) and anonset of neighbourhood competition (Pranchai,2015). The change of morphology from shrub totree architecture was key for this self-rescuingeffect and is a feature distinct from other nurseplant systems, e.g., from alpine regions (Schöbet al., 2014), where nurse plants are not conspe-cifics of the facilitated plants.

17.3.4 Faunal Facilitation of SeedlingRecruitment

While plant interactions dominate the literatureon facilitation during colonisation of new areas,the effects of fauna become increasingly apparentas forests mature. The burrowing and sedimentfeeding activities of crabs, mud shrimps and mudskipper fish collectively transform what wouldhave been a relatively flat forest floor into avariable-height topography of burrow diggingspills, burrow ‘hoods’ and burrow openings.

Minchinton (2001) speculated that such topog-raphy provides opportunity for propagules tobecome trapped on the forest floor during tidalflooding. Burrow mounds were particularlycommon under canopy cover, accounting for upto 44 per cent of the forest floor. Minchinton(2001) found that 75 per cent more propaguleswere trapped in areas with mounds than thosewithout, and that propagules were more likely toestablish as seedlings when growing on mounds.The establishment of seedlings was also faster onmounds than on flats (Minchinton, 2001), pos-sibly as the window of opportunity for propagulesettlement (sensu Balke et al., 2011) is extended bythe amelioration of hydrological stress by eleva-tion in surface topography. The study showedcrab burrowing can have a positive effect on man-grove recruitment in mature forests and in forestgaps and might aid in the recovery of forests afterdisturbance events. Crabs are also avid propagulepredators (Sousa and Dangremond, 2011) and theeffective outcome of crabs on seedling establish-ment is likely to be dependent on contextualvariation in offsetting of propagule trappingagainst propagule predation. Nevertheless, theeffect of crab mounds on propagule establish-ment is similar to that offered by mussels in theestablishment of salt marsh vegetation. Angeliniet al. (2015) found that mussel patches, whichaccount for a much smaller proportion of marsharea cover than do crab burrows in mangroves,had significant and large-scale facilitating impli-cations for marsh functioning, including theboosting of primary production.

17.4 Early Growth – Facilitation inSeedlings and Saplings

17.4.1 Sedimentation and Nutrient SupplyPositive density-dependent effects operating oversmall scales may persist well beyond the initialestablishment and growth of mangrove seed-lings, although the mechanisms causing thisintra- and inter-specific facilitation are likely tochange as plants mature. In Sri Lanka, R. mucro-

nata seedlings planted at high densities grewfaster and showed better survival than those at




www.cambridge.org



low densities (Kumara et al., 2010), an effect thatpersisted for at least six years (Kumara, personalcommunication). Thampanya et al. (2002) alsorecorded positive effects of density on the samespecies in Thailand. Macronutrients, in particularnitrogen and phosphorus, are typically limitingfactors of mangrove growth (Alongi, 2009), andbiophysical processes that enhance the deliveryand absorption of nutrients will usually improvegrowth. In the Sri Lanka case, denser stands oftrees accumulated more allocthonous sedimentwith high nitrogen content and this was thelikely cause of the better performance of high-density plants (Phillips et al., 2017).

17.4.2 Associational Resistance toHerbivores

A plant’s spatial associations with other plantscan alter its detection by and/or vulnerability toherbivores. Interspersion of a host plant withother species can decrease (associational resist-ance) or increase (associational susceptibility) itsherbivore load, compared to what it experienceswhen growing in monospecific stands (Barbosaet al., 2009). To our knowledge, the beneficialeffects of associational resistance to herbivoryhave not been studied explicitly in mangrove eco-systems. This may be a consequence of the long-standing belief that mangrove vegetation is struc-tured primarily by responses of plants to physicaland chemical, rather than biological, stressors.The apparent low rates of folivory in mangrovescompared to terrestrial forests has reinforced thisview (Komiyama et al., 2008; Alongi, 2009). How-ever, most estimates of folivore damage to man-groves are based on the level of standing leafdamage, which has been shown to greatly under-estimate true rates of loss, since leaves that arecompletely consumed are not included in theestimates. When Burrows (2003) marked individ-ual leaf buds and followed their fates to maturity,he estimated leaf damage of 5–8.3 per cent forRhizophora stylosa and 19.3–29.5 per cent for Avi-

cennia marina, substantially higher than earlierestimates based on standing leaf damage. In add-ition, other, less obvious, herbivorous niches,such as stem wood-borers, are functionallyimportant in mangroves and typically are over-looked when estimating biomass lost to

herbivory. For example, stem-boring beetleskilled more than 50 per cent of a fringing Rhizo-

phora mangle canopy on offshore islands in Belize(Feller and McKee, 1999; Feller, 2002). Hence, it isclear that mangrove stands must cope with boththe stressful chemical and physical conditionsalready discussed and the biological stressimposed by herbivore damage comparable to thatobserved in other types of forests.

Associational resistance has been well-documented in terrestrial vegetation. Amongthe first studies to experimentally demonstrateit were Root and colleagues’ investigations ofherbivore–plant interactions in gardens plantedinto old field habitat (Tahvanainen and Root,1972; Root, 1973), which showed an inverse rela-tionship between herbivore load on collard (Bras-sica oleracea) and the diversity of neighbouringvegetation (pure stands of collard versus a diversemix of meadow grasses and forbs). Alternative(but not mutually exclusive) mechanisms thatcould account for this relationship include: (1)the enemies hypothesis: diverse vegetation har-bours a greater number of natural enemies ofherbivores (predators and parasitoids) thansingle-species stands and (2) the resource concen-tration hypothesis: a host plant is more likely tobe found, particularly by specialist herbivores, ifit grows in a dense monoculture of conspecificsthan in a mixed-species stand, and such herbi-vores are more likely to aggregate and reproducein these areas of high resource availability andare less likely to emigrate from them (Root, 1973;Bach, 1980). Since the publication of this classicgarden-meadow study, associational resistance toherbivores has been experimentally demon-strated in a variety of natural communities,including nearshore marine habitats (e.g., Pfisterand Hay, 1988), open woodlands with shrubunderstory (Baraza et al., 2006) and shorelinevegetation (Hambäck et al., 2000).

As described earlier, the resource concentra-tion hypothesis posits that a host plant is atgreater risk of herbivory when growing in amonoculture than in a mixed-species stand, par-ticularly if it is primarily fed on by specialists.However, an increase in local density withinmonocultures could lower the per capita risk ofattack if the herbivore does not exhibit a




www.cambridge.org



sufficient numerical response (through behav-ioural aggregation or in situ reproduction) tokeep pace with plant growth or compensatoryrecovery from herbivore damage. In effect, asthe local density of host plants increases, theresident herbivore population becomesswamped/satiated and per capita rates of damageand mortality decline (Crawley, 1997; Otwayet al., 2005). This is more likely to occur if thespecialist herbivore is univoltine (i.e., a singlebrood of offspring per year), has low fecundityand/or a complex life cycle, with a grazing larvalstage that metamorphoses into a mobile, non-grazing adult stage (e.g., Lepidoptera). In thelatter instance, the reproductive adult dispersesaway from the host plant and is unlikely toreturn to lay eggs in the same patch of plants inwhich it grazed as a larva (Cromartie, 1975).

As noted earlier, we know of no publishedinvestigations that specifically test for associ-ational resistance to herbivory in mangrove habi-tats. The study that comes closest is Johnstone’s(1981), which quantified rates of standing insectgrazing damage to mature leaves of twenty-threemangrove species growing in mixed stands incoastal swamps of the Port Moresby region ofPapua New Guinea. He found no relationshipbetween rates of herbivory and the speciesrichness of mangroves growing within 25 m ofthe sampled tree, and no correlation betweenleaf area eaten and the densities of individualspecies. However, patterns could have beenobscured by large species-specific variation in sus-ceptibility among the twenty-three species hesampled.

New evidence that associational resistance toherbivory occurs in mangroves comes from anunpublished field experiment that one of us(Sousa) conducted to assess the roles of intra-and inter-specific competition on growth and sur-vival of mangroves along the tidal gradient on thecentral Caribbean coast of Panama. In this experi-ment, young (~ 1-month-old) mangrove seedlingsof the three canopy mangrove species A.

germinans, Laguncularia racemosa and R. mangle

were planted into single- and mixed-species treat-ments, both inside and outside of replicatecanopy gaps created by past lightning strikes.The complete design and results of this study will

be reported elsewhere; here we focus on patternsof survivorship of A. germinans seedlings as a func-tion of density and species composition insidethree upper-intertidal gaps, within forest standsdominated by conspecific adults. These stands arewhere populations of the specialist lepidopteranJunonia genoveva, or black mangrove buckeye, areconcentrated (Sousa, unpublished data). J. geno-veva larvae feed exclusively on the leaves of A.germinans and can strongly impact seedling popu-lations (Elster et al., 1999). We analysed rates ofsurvival over the first six months of the experi-ment; young seedlings are the most attractive lifestage to egg-laying, adult J. genoveva, and are themost likely stage to be killed by their larvae(Sousa, unpublished data).

The experiment yielded evidence of bothherbivore swamping by high host plant densityand interspecific associational resistance(Figure 17.3). Survival rates differed significantlyamong treatments (F5,12 = 12.72, P = 0.0019).Among the A. germinans monocultures, the meanrate of survival was higher in the three-fold dens-ity treatment than either the two-fold or one-foldseedling densities. Survival was also higher in the1:1 and 1:2 mixed treatments than the one-folddensity monoculture, which contained the samenumber of A. germinans seedlings, a pattern indi-cative of associational resistance. Survival in the2:1 mixed treatment appeared to be greater thanin the two-fold monoculture, also suggestive ofassociational resistance, but the difference wasnot significant (P = 0.095).

This experiment did not directly manipulate J.genoveva densities to confirm that grazing by itslarvae was responsible for seedling mortality. Wedid observe numerous larvae feeding on theplants and many adult butterflies flying aroundthe study forests, laying eggs on host plants. In asubsequent experiment of similar design, anherbivore-exclusion treatment was added; it con-firmed that J. genoveva caterpillars are responsiblefor most of the mortality of young A. germinans

seedlings in upper-intertidal basin forests, wherethis experiment was conducted.

The specific mechanisms accounting for asso-ciational resistance in this system are not known.The presence of neighbouring non-host plantsmay physically interfere with the adult




www.cambridge.org



butterfly’s ability to locate and oviposit on a hostplant. In addition, A. germinans leaves containiridoid glycosides (Fauvel et al., 1995). This classof chemical compounds has been shown to actas oviposition stimulants for J. genoveva’s temper-ate zone congener, Junonia coenia (Pereyra andBowers, 1988); therefore, it is conceivable thatthere may also be some interference withchemical signalling in patches of mixed-speciescomposition.

17.5 Mature Trees and Forests

17.5.1 Faunal Enhancement of MangrovePrimary Production

There is good evidence that crabs facilitate man-grove production. Removing crabs from the ben-thos of Rhizophora-dominated stands in Australialed to a reduction in forest primary productionand reproductive output (Smith et al., 1991); anoutcome that is very similar to the result of crabexclusion experiments in salt marshes (Bertness,1985). Bioturbation by crabs aerates mangrovesoils and reduces soil sulphide content (Smithet al., 1991), a chemical that depresses the pri-mary productivity of coastal wetland plants ingeneral (Bertness, 1985). Burrowing by crabs alsoregulates other soil characteristics that influenceforest production. Smith et al. (2009) found thatfield exclusion of fiddler crabs reduced thegrowth of L. racemosa seedlings, probably becausesoil salinity rose in the absence of crabburrowing. Faunal burrows aid the flushing ofsediments by tidal water (Stieglitz et al., 2013),which dilutes salinity and reduces sulphatereduction (Kristensen, 2000; Smith et al., 2009).Crab burrowing is also thought to boost nitrifica-tion and thereby plant growth (Bertness, 1985),and Skov and Hartnoll (2002) proposed thatselective feeding of crabs on mangrove leaf litterfacilitates the retention and remineralisation oflitter nutrients for the benefit of crabs them-selves, as well as forest productivity. So far, theexperimental evidence of this happening incoastal wetlands is limited (Daleo et al., 2007;Kristensen et al., 2008).

Crab burrowing might also indirectly enhanceforest production by facilitating the activity ofother species that stimulate tree growth. In saltmarshes, the aeration of soils by crab burrowingfacilitated the development of mycorrhizalfungi, which boost the availability of nitrogenfor plant production (Daleo et al., 2007). Thefungi need soil aeration to grow and the removalof crabs, and their burrows, reduced thegrowth of salt marsh Spartina plants by 35 percent (Daleo et al., 2007). Mycorrhizal fungi areabundant in the soils of coastal wetlands (Car-valho et al., 2004), and it is likely that crab

Figure 17.3 Survival to six months of A. germinans (A)

seedlings planted in three monospecific treatments of one-,

two- and three-fold density (A, AA, AAA), and three mixed-

species treatments of 1:1 (AX), 1:2 (AXX) and 2:1 (AAX)

density combinations of A. germinans with one of two other

mangrove species (X = L. racemosa or R. mangle). Treatments

were established in 0.5 m2 plots at densities of twenty-five,

forty and eighty-one seedlings per plot; the design was

replicated inside three upper-intertidal gaps. The three mixed-

species treatments contained twenty-five, twenty-seven and

fifty-four A. germinans seedlings, respectively. Survival values for

the pair of plots (one with L. racemosa and the other with R.

mangle) that contained a 1:1, 1:2 or 2:1 ratio treatment were

averaged for the analysis. Because seedlings in one of the gaps

suffered nearly four-times higher mortality across all

treatments than the other two, we standardised the proportion

surviving values from each gap by converting them to z-scores,

based on the respective gap means and standard deviations.

Open symbols ( ⃝, ∆, ⃞) represent values from the three

replicate light gaps. TheL

symbol marks the mean Z-score of

the three replicates. Letters to the right of these symbols

summarize results of a Tukey honest significant difference test;

those not sharing a letter are significantly different at P < 0.05.

The mean proportions alive at six months in each of the six

treatments are presented just above the x-axis. SE,

standard error.




www.cambridge.org



facilitation of mycorrhiza will also boost man-grove tree production.

Exclusion of crabs does not always result in areduction of tree growth. A year-long removal ofa dominant semi-terrestrial crab from a high-shore Rhizophora stand in Brazil did not haveany measurable impact on forest growth (Pül-manns et al., 2016). While the lack of effectmight be because crab removal was not complete(approximately a third of all crabs wereremoved), it may equally well be that the facil-itatory role of crabs in forest production iscontext-dependent and influenced by a range ofgeomorphological, physio-chemical, seasonal orbiological factors (Pülmanns et al., 2016). Theor-etical and empirical work emphasises the influ-ence of environmental context on the relativeimportance of facilitation, particularly along gra-dients of stress (Bruno et al., 2003; Maestre et al.,2009; Schöb et al., 2014). The influence of stressgradients on faunal facilitation has not beenaddressed in mangroves.

While the evidence for crab facilitation ofmangrove production is considerable, otherfauna can also positively affect forest production.Ellison and colleagues (Ellison and Farnsworth,1990; Ellison et al., 1996) described an intriguingfacultative mutualism between Rhizophora treesand their prop root-colonising sponges. Treesfringing creeks in Belize, with permanently sub-merged roots, grew adventitious rootlets withinsponge tissues to extract nitrogen from sponges.Sponges in return were offered colonisation sub-strate as well as organic carbon by the trees andboth organisms grew substantially faster whencoexisting. Facilitation may also be instigated byvertebrates. For example, birds can boost treeproduction through providing growth-limitingnutrients. Mangroves offer preferential roostingsites to many bird species that feed on adjacentmudflats (Buelow and Sheaves, 2015). Birdroosting sites may be restricted to select areas ofthe forest, the preference for which may last foryears (Pearse, 2010). Bird guano in such habitualroosting areas can offer a locally significant andsteady supply of nutrients that ultimately boosttree growth (Onuf et al., 1977; Feller, 1995).

17.5.2 Indirect Protection fromHerbivores by Epibionts orPredators

A variety of indirect ecological interactions havebeen shown to reduce the negative impacts ofstem-borers on mangrove prop roots and foli-vores on mangrove leaves. Mats of epibionts,comprised of colonial ascidians and sponges,commonly grow on the surfaces of submergedyoung R. mangle prop roots. As described earlier,these may include organisms that lesson thechemical stress of nutrient limitation throughmutualistic associations, and they can also affectbiological stresses by deterring attacks by stem-boring isopods (Ellison and Farnsworth, 1990,1992). The mechanism(s) by which an encrustinglayer of ascidians and sponges blocks isopods isunknown; it may act as a physical and/or chem-ical barrier to their recruitment and boringactivity.

Emergent portions of mangrove trees may beindirectly protected from insect herbivory byassociated predators, including ants and lizards.In these tri-trophic interactions, the predatorsreduce the density of insect herbivores, indirectlybenefitting the plant. Mangrove protection byants is well documented, with examples fromboth comparative and experimental studies.Ozaki et al. (2006) compared rates of predationon populations of the scale insect, Aulacaspis

marina (Homoptera: Diaspidodae) infesting pottedseedlings of R. mucronata introduced into maturenatural forests and young plantations growing inabandoned shrimp ponds, on Bali Island, Indo-nesia. In the natural forests, two species of ants(Monomorium floricola and Paratrechina sp.) preyedheavily on the scale insects, suppressing theirdensity by 88 per cent in seven days. By compari-son, only 28 per cent were eaten in the plantationsites, probably because the young trees in thesesites afforded few ant nesting sites and the inun-dated soils prohibited ants from nesting in theground. A second experiment in which ants wereexcluded from half the seedlings with sticky bar-riers applied to their lower stem confirmed thatants accounted for almost all the scale insectmortality.




www.cambridge.org



Offenberg et al. (2004) documented a negativecorrelation between the density of arborealweaver ants (Oecophylla smaragdina) and levels ofherbivory on R. mucronata leaves in a Thai man-grove forest. Trees lacking ants had more thanthree times the herbivore leaf damage of treeswith ant nests. On trees with ants, leaves nearthe nest suffered less damage than those in otherareas of the canopy. Most of the leaf damage wascaused by chrysomelid beetles and sesarmidcrabs; both were deterred by the presence of ants,and ants were observed preying on the beetles. Inthis case, the relationship might be considered aweak form of ant–plant mutualism, since theants weave the host mangrove leaves together tobuild their nest (Offenberg et al., 2004). Weaverants have long been used for herbivorous insectpest control in a variety of tree crop systems (VanMele, 2008). An earlier study of insect herbivoryrates in a Papua New Guinea mangrove forest(Johnstone, 1981) did not detect a statisticallysignificant relationship between standing leafdamage and the presence of O. smaragdina

colonies. While the mean percent of leaf areaeaten tended to be higher on trees that had noants, compared to those with ant colonies, therewas high variation in herbivory rates among treeswith similar densities of ants. The difference inthe findings of Offenberg et al. (2004) and John-stone (1981) likely stems from a fundamentaldifference in method. The former study focussedon a single host plant species that is frequentlyoccupied by weaver ants, while the latter com-pared rates for a pooled sample of leaves fromtwenty-three different species of mangroves,which varied in their attractiveness to the ants.This undoubtedly introduced considerable vari-ation in other leaf attributes that affect rates ofherbivory.

Ants also play a defensive role on small Baha-mian islands, where the buttonwood mangrove,Conocarpus erectus, dominates the shoreline vege-tation. This plant has extrafloral nectaries thatattract a variety of insects, including nine speciesof ants. Its leaves come in two morphs, a silverform that has a dense layer of leaf hairs or trich-omes on their surface, and a green form that hasvery few trichomes. Trichomes function as astructural defence against folivorous insects

(Schoener, 1987, 1988; Agrawal and Spiller,2004); silver plants have fewer extrafloral nectar-ies than green plants, and they produce lessnectar and attract fewer ants (Piovia-Scott,2011). Experimental exclusion of ants from low-trichome plants resulted in higher herbivoredamage and lower new leaf production comparedto control plants accessible to ants. In contrast,ant exclusion from silver plants had no measur-able effect of either leaf damage or leaf produc-tion (Piovia-Scott, 2011). Anolis lizards also preyon insect folivores of C. erectus on these islands;some islands support lizard populations andothers lack them. In a survey of seventy-fourislands, total leaf damage was 42–59 per centgreater on no-lizard- than lizard-inhabited islands(Schoener, 1988).

17.5.3 Facilitation Cascades and theScaling-Up of Faunal Facilitationof Mangroves

Mangrove trees act as foundation species, creat-ing complex habitats that support multiple otherspecies which together constitute the mangroveecosystem. When an independent foundationspecies supports other, dependent foundationspecies, which themselves facilitate the survivalof different organisms, a facilitation cascade mayensue, with facilitatory effects rippling betweentrophic levels (Angelini et al., 2011). Bishop et al.(2012) describe such a cascade in Avicennia marina

forest, where beyond a threshold density of pneu-matophores capture of algae facilitate fauna thatdepend on algae to ameliorate environmentalstressors, including desiccation risk. Such facili-tatory cascades may have profound implicationsfor ecosystem functioning, when the array offacilitated species has distinct functional roles.Angelini et al. (2015) found that colonisation bymussels, which are secondary foundation speciesin North American salt marshes, facilitated anarray of species that together stimulated marshaccretion, carbon sequestration, marsh grass pro-duction and faunal functional richness. Crabscould be argued to have a similar secondary foun-dation role in mangroves, potentially leading tofaciliatory cascades of benefit to trees. Theirfacilitation of other organisms is certainlydiverse, from providing habitat to other




www.cambridge.org



invertebrates, to facilitating the growth of mycor-rhizal fungi and microphytobenthic species(Alongi, 1994; Gillikin et al., 2001; Daleo et al.,2007). Predatory as well as herbivorous crabs mayact as facilitators. An observed reduction in saltmarsh plant production in the USA has beenattributed to 40–80 per cent reductions in preda-tory blue crab and fish populations and theirnatural control of herbivorous snails and crabs(Altieri et al., 2012). So far, there is no firm evi-dence of fauna regulating facilitation cascades inmangroves, but the likelihood of it occurringis high.

17.6 Forest Resilience in the Face ofLong-Term Change

The intertidal zone is a place of daily, seasonaland decadal flux. Colonising new areas inresponse to long-term change, driven for exampleby sea-level rise (SLR) or altering river flows,allows mangroves to adapt. This spatially basedresilience relies in part on the facilitative mech-anisms discussed earlier; the ability for pioneerplants to exploit windows of opportunity in baresubstrate, often supported by interactions withother organisms. But there are many locationswhere the prospects for forest migration, inshoreor offshore, are limited; for example, some man-groves grow on coral islands with no hinterlandand forests are increasingly restricted frommove-ment in-land by anthropogenic structures andactivities. The absence of room to move doesnot, however, mean that a mangrove forest lacksresilience and the ability to persist over time. Forexample, Caribbean mangroves growing in areaswithout alluvial deposits and with limited oppor-tunities to move spatially are able to adjust torising sea level through the deposition of organicmatter, with some now growing on 10 m of peatrepresenting thousands of years of adjustment(McKee et al., 2007a). This ability of mangrovesto elevate their soil surfaces in response to risingsea levels relies on a large range of factors, includ-ing the above- and below-ground productivitystimulated by fauna and the sediment trappingassisted by conspecific density (Krauss et al.,

2014), and burrowing crabs may also be import-ant agents in helping to store organic carbonbelow ground (Andreetta et al., 2014).

Hence, facilitatory processes assist in the long-term persistence of mangroves and contribute tothe enormous carbon density of these forests(Figure 17.4). Change (over space and time) is acentral feature of mangrove systems. Over thepast twenty years, the paradigm of ‘balance ofnature’ has largely been replaced among ecolo-gists by ‘resilience thinking’ (Walker and Salt,2012), but conservation of the status quo is stilla common goal for managers and the broaderconservation movement. A focus on resiliencemechanisms is essential to identify the relevantspatial and temporal scales at which ‘self-similar-ity’ (Jax et al., 1998), ‘integrity’ (Cumming andCollier, 2005) and ‘persistence of relationship’(Holling, 1973) self-guard ecosystem functioning.

17.7 Conclusions

Benignity is seldom found in alliancewith strength.

Alexander von Humbolt

The SGH suggests that searching for facilitationwithin mangrove ecosystems should be fruitful;these forests are miracles of productivity andpersistence in the face of the multiple stressesthat they naturally face. Our brief review con-firms this prediction. Facilitation can be foundat all stages of the lives of individual trees andof the forest ecosystems themselves. Whilereports of the amelioration of physical and chem-ical stresses predominate, we also present evi-dence of how facilitative interactions can helplimit the biological stress of herbivory. Whatremains unclear, however, is whether thesediverse observations can inform a coherenttheory of facilitation in mangrove ecosystems.While the complex interplay of plant diversity,density and environmental stressors in creatingcontext-specific outcomes is slowly being under-stood in other, much simpler, plant commu-nities, such as alpine cushion plants (Schöbet al., 2014), a comparable understanding of




www.cambridge.org



contingent ecological outcomes that structuremangrove communities is yet to emerge. In part,this is because we are still in the process of dis-covering how these unique forests work. Modernmethods of ecological research, particularlymanipulative field experiments and mathemat-ical as well as computative modelling, have beenapplied for a much shorter time and by fewerinvestigators in mangroves than in terrestrialhabitats. Not surprisingly, new findings fre-quently contravene standard explanationsderived from studies in other ecosystems. Man-groves contain pronounced stress gradients onrelatively compact spatial scales. These gradientsconsist both of resources (e.g., nitrogen or phos-phorous) and of non-resources (e.g., salinity ortemperature). Mangrove flora and fauna mustcope with multiple, interacting stress factorsand all species vary in their stress tolerance andcompetitiveness. These factors make mangrovesystems difficult to understand. But they alsomean that mangroves provide an extraordinarylaboratory for building a more comprehensiveand general understanding of the role that facili-tation and other processes play in structuringcommunities. Achieving this will require a coord-inated and hypothesis-driven effort to experimen-tally disentangle the predictions of the refinedstress-gradient hypothesis (Maestre et al., 2009)and its extensions by considering the interactiveinfluences of abiotic and biotic processes across arange of environment settings. Mangroveresearchers will need to work together to do this –therefore combine, and practice mutual aid.

Acknowledgements

We thank Sarah Murray for her help with thefigures and Louise Firth for useful editing sugges-tions. We were inspired by opportunities to meet

Figure 17.4 The accumulation of carbon in the R. mucronata

forest of Gazi Bay, helping with resilience of the forest in the

face of SLR and resulting from multiple forms of facilitation.

There are four main components of the long-term (years,

decades or longer) carbon pool: (a) (clockwise from top-left)

soil organic carbon, above-ground biomass, below-ground

biomass (living roots) and dead root materials. (b) These four

pools, in the same order, but here represented as the

percentage contribution to the total pool at Gazi, with soil

organic carbon constituting 95 per cent of the total (data from

Tamooh et al., 2008; Cohen et al., 2013; Gress et al., 2017;

figures converted to t C ha-1 equivalents, assuming carbon

content of living roots, dead roots and living stems of 0.39, 0.5

and 0.47, respectively). (c) Surface elevation measured in ten

plots from Gazi over fifty-eight months, showing 3.1 mm

elevation per year, driven by below-ground accumulation of

carbon.




www.cambridge.org



and share ideas at the Aquatic Biodiversity andEcosystems Conference in 2015 and the Man-grove and Macrobenthos Meeting 4 in 2016;thank you to all those who organised these meet-ings and invited us.

REFERENCES

Agrawal, A. A. and Spiller, D. S. (2004). Polymorphicbuttonwood: effects of disturbance on resistance toherbivores in green and silver morphs of a Bahamianshrub. American Journal of Botany, 91, 1990–7.

Alongi, D. M. (1994). Zonation and seasonality of ben-thic primary production and community respirationin tropical mangrove forests. Oecologia, 98, 320–32.

Alongi, D. M. (2008). Mangrove forests: resilience, pro-tection from tsunamis, and responses to global cli-mate change. Estuarine, Coastal and Shelf Science, 76,1–13.

Alongi, D. M. (2009). The Energetics of Mangrove Forests,Springer, Dordrecht.

Altieri, A. H., Bertness, M. D., Coverdale, T. C., Herr-mann, N. C. and Angelini, C. (2012). A trophiccascade triggers collapse of a salt-marsh ecosystemwith intensive recreational fishing. Ecology, 93,1402–10.

Andreetta, A., Fusi, M., Cameldi, I., Cimò, F., Carnicelli,S. and Cannicci, S. (2014). Mangrove carbon sink. Doburrowing crabs contribute to sediment carbon stor-age? Evidence from a Kenyan mangrove system. Jour-nal of Sea Research, 85, 524–33.

Angelini, C., Altieri, A. H., Silliman, B. R. and Bertness,M. D. (2011). Interactions among foundation speciesand their consequences for community organization,biodiversity, and conservation. BioScience, 61, 782–9.

Angelini, C., van der Heide, T, Griffin, J. N. et al. (2015).Foundation species’ overlap enhances biodiversityand multifunctionality from the patch to landscapescale in southeastern United States salt marshes. Pro-ceedings of the Royal Society B, 282, 20150421.

Bach, C. E. (1980). Effects of plant diversity and time ofcolonization on an herbivore-plant interaction. Oeco-logia, 44, 319–26.

Balke, T., Bouma, T. J., Horstman, E. M., Webb, E. L.,Erftemeijer, P. L. A. and Herman, P. M. J. (2011).Windows of opportunity: thresholds to mangroveseedling establishment on tidal flats. Marine Ecology

Progress Series, 440, 1–9.Baraza, E., Zamora, R. and Hódar, J. A. (2006). Condi-tional outcomes in plant-herbivore interactions:neighbours matter. Oikos, 113, 148–56.

Barbier, E. B., Koch, E. W., Silliman, B. R. et al. (2008)Coastal ecosystem-based management with nonlinearecological functions and values. Science, 319, 321–3.

Barbosa, P., Hines, J., Kaplan, I., Martinson, M., Szcze-paniec, A. and Szendrei, Z., (2009). Associationalresistance and associational susceptibility: havingright or wrong neighbors. Annual Review of Ecology

Evolution and Systematics, 40, 1–20.Bertness, M. D. and Callaway, R. (1994). Positive inter-actions in communities. Trends in Ecology & Evolution,9, 191–3.

Bertness, M. D. (1985). Fiddler crab regulation of Spar-tina alterniflora production in a New England saltmarsh. Ecology, 66, 1042–55.

Bishop, M. J., Byers, J. E., Marcek, B. J. and Gribben, P. E.(2012). Density-dependent facilitation cascades deter-mine epifaunal community structure in temperateAustralian mangroves. Ecology, 93, 1388–401.

Bruno, J. F., Stachowicz, J. J. and Bertness, M.D. (2003).Inclusion of facilitation into ecological theory. Trendsin Ecology and Evolution, 18, 119–25.

Buelow, C. and Sheaves, M. (2015). A birds-eye view ofbiological connectivity in mangrove systems. Estuar-ine, Coastal and Shelf Science, 152, 33–43.

Burrows, D. W. (2003). The role of insect leaf herbivoryon the mangroves Avicennia marina and Rhizophorastylosa. PhD thesis, James Cook University.

Carvalho, L. M., Correia, P. M. and Martins-Loucão, M.A. (2004). Arbuscular mycorrhizal propagules in asalt marsh. Mycorrhiza, 14, 165–70.

Chapin, F. S, Autumn, K. and Pugnaire, F. (1993). Evo-lution of suites of traits in response to environmentalstress. American Naturalist, 142, S78–92.

Clements, F. E. (1916). Plant Succession: An Analysis of the

Development of Vegetation. Carnegie Institution ofWashington, Washington, DC.

Cohen, R., Kaino, J., Okello, J. A. et al. (2013). Propagat-ing uncertainty to estimates of above-ground bio-mass for Kenyan mangroves: a scaling procedurefrom tree to landscape level. Forest Ecology and Man-

agement, 310, 968–82.Connell, J. H. and Slatyer, R. O. (1977). Mechanisms ofsuccession in natural communities and their role incommunity stability and organisation. The American

Naturalist, 111, 1119–44.Crawley, M. J. (1997). Plant–Herbivore Dynamics. In M.J. Crawley, ed. Plant Ecology, second edn. BlackwellScientific Publications, Oxford, pp. 401–73.

Cromartie, W. J., Jr. (1975). The effect of stand size andvegetational background on the colonization of cru-ciferous plants by herbivorous insects. Journal of

Applied Ecology, 12, 517–33.




www.cambridge.org



Cumming, G. S. and Collier, J. (2005). Change and iden-tity in complex systems. Ecology and Society, 10, 29.

Daleo, P., Fanjul, E., Casariego, A. M., Silliman, B. R.,Bertness, M. D. and Iribarne, O. (2007). Ecosystemengineers activate mycorrhizal mutualism in saltmarshes. Ecology Letters, 10, 902–8.

Ellison, A. M, Farnsworth, E. J and Twilley, R. R. (1996).Facultative mutualism between red mangroves androot-fouling sponges in Belizean mangal. Ecology, 77,2431–44.

Ellison, A. M. and Farnsworth, E. J. (1990). The ecologyof Belizean mangrove-root fouling communities I:epibenthic fauna are barriers to isopod attack of redmangrove roots. Journal of Experimental Marine Biology

and Ecology, 142, 91–104.Ellison, A. M. and Farnsworth, E. J., (1992). The ecologyof Belizean mangrove-root fouling communities II:patterns of epibiont distribution and abundance,and effects on root growth. Hydrobiologia, 247, 87–98.

Elster, C., Perdomo, L., Polania, J. and Schnetter, M-L.,(1999). Control of Avicennia germinans recruitmentand survival by Junonia evarete larvae in a disturbedmangrove forest in Columbia. Journal of Tropical Ecol-ogy, 15, 791–805.

Fauvel, M-T., Bousquet-Melou, A., Moulis, C., Gleye, J.and Jensen, S. R. (1995). Iridoid glucosides in Avicen-

nia germinans. Phytochemistry, 38, 893–4.Feller, I. C. (1995). Effects of nutrient enrichment ongrowth and herbivory of dwarf red mangrove (Rhizo-phora mangle). Ecological Monographs, 65, 477–505

Feller, I. C. and McKee, K. L. (1999). Small gap creationin Belizean mangrove forests by a wood-boringinsect. Biotropica, 31, 607–17.

Feller, I. C. (2002). The role of herbivory by wood-boringinsects in mangrove ecosystems in Belize the role ofherbivory by wood-boring insects in mangrove eco-systems in Belize. Oikos, 97, 167–76.

Gedan, K. B. and Silliman, B. R. (2009). Using facilita-tion theory to enhance mangrove restoration. Ambio,38, 109.

Gillikin, P.G., de Grave, S. and Tack, J. F. (2001). Theoccurrence of the semi-terrestrial shrimp Merguia

oligodon (de Man, 1888) in Neosaramatium smithi

H. milne Edwards, 1853, burrows in Kenyan man-groves. Crustaceana, 74, 505–7.

Gress, S, Huxham, M., Kairo, J., Mugi, L. and Briers, R.(2017). Evaluating, predicting and mapping below-ground carbon stores in Kenyan mangroves. GlobalChange Biology, 23(1), 224–34, http://dx.doi.org/10.1111/gcb.13438.

Guo, H., Zhang, Y., Lan, Z. and Pennings, S. C. (2013).Biotic interactions mediate the expansion of black

mangrove (Avicennia germinans) into salt marshesunder climate change. Global Change Biology, 19,2765–74.

Hambäck, P. A., Ågren, J. and Ericson, L. (2000). Associ-ational resistance: insect damage to purple loose-strife reduced in thickets of sweet gale. Ecology, 81,1784–94.

He, Q. and Bertness, M. D. (2014). Extreme stresses,niches, and positive species interactions along stressgradients. Ecology, 95, 1437–43.

He, Q., Bertness, M. D. and Altieri, A. H. (2013) Globalshifts towards positive species interactions withincreasing environmental stress. Ecology Letters, 16,695–706.

Holling, C. S. (1973). Resilience and stability of eco-logical systems. Annual Revue of Ecology and Systemat-

ics, 4, 1–23.Huxham, M., Emerton, L., Kairo, J. et al. (2015). Apply-ing climate compatible development and economicvaluation to coastal management: a case study ofKenya’s mangrove forests. Journal of Environmental

Management, 157, 168–81.Huxham, M., Kumara, M. P., Jayatissa, L. P. et al. (2010).Intra- and interspecific facilitation in mangrovesmay increase resilience to climate change threats.Philosophical Transactions of the Royal Society B: Biological

Sciences, 365, 2127–35.Jayatissa, L. P., Wickramasinghe, W. D. L., Dahdouh-Guebas, F. and Huxham, M. (2008). Interspecific vari-ations in responses of mangrove seedlings to twocontrasting salinities. International Review of Hydrobiol-

ogy, 93, 700–10.Jax, K., Jones C. and Pickett, S. (1998). The self-identityof ecological units. Oikos, 82, 253–64.

Johnstone, I. M. (1981). Consumption of leaves by herbi-vores in mixed mangrove stands. Biotropica, 13,252–9.

Kirui, B. Y. K., Huxham, M., Kairo, J. and Skov, M.(2008). Influence of species richness and environ-mental context on early survival of replantedmangroves at Gazi bay, Kenya. Hydrobiologia, 603,171–81.

Kodikara, K. A. S., Mukherjee, N., Jayatissa, L. P., Dah-douh-Guebas, F. and Koedam, N. (2017). Have man-grove restoration projects worked? An in-depth studyin Sri Lanka. Restoration Ecology, 25(5), 705–16.

Komiyama, A., Ong, J. E. and Poungparn, S. (2008).Allometry, biomass, and productivity of mangroveforests: a review. Aquatic Botany, 89, 128–37.

Krauss, K. W., Mckee, K. L., Lovelock, C. E. et al. (2014).How mangrove forests adjust to rising sea level. NewPhytologist, 202, 19–34.




www.cambridge.org



Krebs, C. (2001). Ecology: The Experimental Analysis of

Distribution and Abundance, fifth edn. Benjamin Cum-mings, New York.

Kristensen, E. (2000). Organic Matter Diagenesis at theOxic/Anoxic Interface in Coastal Marine Sediments,with Emphasis on the Role of Burrowing Animals. InG. Liebezeit, S. Dittmann and I. Kröncke, eds. Life atInterfaces and Under Extreme Conditions: Developments in

Hydrobiology. Springer, Dordrecht.Kristensen, E., Buillon, S., Dittmar, T. and Marchand, C.(2008). Organic carbon dynamics in mangrove eco-systems: a review. Aquatic Botany, 89, 201–19.

Kumara, M. P., Jayatissa, L. P., Krauss, K. W., Phillips, D.H. and Huxham, M. (2010). High mangrove densityenhances surface accretion, surface elevationchange, and tree survival in coastal areas susceptibleto sea-level rise. Oecologia, 164, 545–53.

Maestre, F. T., Callaway, R. M., Valladares, F. and Lortie,C. J. (2009). Refining the stress-gradient hypothesisfor competition and facilitation in plant commu-nities. Journal of Ecology, 97, 199–205.

Mazda, Y., Michimasa, M., Kogo, M. and Hong, P. N.(1997). Mangroves as coastal protection from wavesin the Tong King delta, Vietnam. Mangroves and Salt

Marshes, 1, 127–35.Mcivor, A., Spencer, T. and Möller, I. (2012). Storm Surge

Reduction by Mangroves, Natural Coastal ProtectionSeries: Report 2. Wetlands International, Nairobi.

McKee, K. L., Cahoon, D. R. and Feller, I. C. (2007a).Caribbean mangroves adjust to rising sea levelthrough biotic controls on change in soil elevation.Global Ecology and Biogeography, 16, 545–56.

McKee, K. L., Rooth, J. E. and Feller, I. C. (2007b). Man-grove recruitment after forest disturbance is facili-tated by herbaceous species in the Caribbean.Ecological Applications, 17, 1678–93.

Mehlig, U., Menezes, M. P. M., Reise, A., Schories, D.and Medina, E. (2010). Mangrove vegetation of theCaete estuary. Mangrove Dynamics and Management in

North Brazil, 211, 71–107.Minchinton, T. E. (2001). Canopy and substratum het-erogeneity influence recruitment of the mangroveAvicennia marina. Journal of Ecology, 89, 888–902.

Munguia, P., Ojanguren, A. F., Evans, A. N. et al. (2009).Is facilitation a true species interaction? The Open

Ecology Journal, 2, 83–5.Offenberg, J., Havanon, S., Aksornkoae, S., Macintosh,D. J. and Nielsen, M. G. (2004). Observations on theecology of weaver ants (Oecophylla smaragdina Fabri-cius) in a Thai mangrove ecosystem and their effecton herbivory of Rhizophora mucronata Lam. Biotropica,36, 344–51.

Onuf, C. P., Teal, J. M. and Valiela, I. (1977). Interactionsof nutrients, plant growth, and herbivory in a man-grove ecosystem. Ecology, 58, 514–26.

Otway, S. J., Hector, A. and Lawton, L. H. (2005).Resource dilution effects on specialist insect herbi-vores in a grassland biodiversity experiment. Journalof Animal Ecology, 74, 234–40.

Ozaki, K., Takashima, S. and Suko, O. (2006). Ant pre-dation suppresses populations of the scale insectAulacaspis marina in natural mangrove forests. Biotro-pica, 32, 764–8.

Pearse, I. S. (2010). Bird rookeries have different effectson different feeding guilds of herbivores and alterthe feeding behavior of a common caterpillar.Arthropod–Plant Interactions, 4, 189–95.

Pereyra, P. C. and Bowers, M.D., (1988). Iridoid glyco-sides as oviposition stimulants for the buckeye, Juno-nia coenia (Nymphalidae). Journal of Chemical Ecology,14, 917–28.

Peters, R., Vovides, A. G., Luna, S., Grüters, U. andBerger, U. (2014). Changes in allometric relations ofmangrove trees due to resource availability – a newmechanistic modelling approach. Ecological Modelling,283, 53–61.

Pfister, C. A. and Hay, M. E. (1988). Associational plantrefuges: convergent patterns in marine and terres-trial communities result from different mechanisms.Oecologia, 77, 118–29.

Phillips, D. H., Kumara, M. P., Jayatissa, L. P., Krauss, K.W. and Huxham, M. (2017). Impacts of mangrovedensity on surface sediment accretion, belowgroundbiomass and biogeochemistry in Puttalam Lagoon,Sri Lanka. Wetlands, 37(3), 471–83, http://dx.doi.org/10.1007/s13157-017-0883-7.

Piovia-Scott, J. (2011). Plant phenotype influences theeffects of ant mutualists on a polymorphic man-grove. Journal of Ecology, 99, 327–34.

Pranchai, A. (2015). Spatial patterns and processes in aregeneratingmangrove forest.Dissertation, TUDresden.

Pülmanns, N., Mehlig, U., Nordhaus, I., Saint-Paul, U.and Diele, K. (2016). Mangrove crab Ucides cordatus

removal does not affect sediment parameters andstipule production in a one year experiment in north-ern Brazil. PLoS ONE 11, e0167375.

Root, R. B. (1973). Organization of a plant-arthropodassociation in simple and diverse habitats: the faunaof collards (Brassica oleracea). Ecological Monographs,43, 95–124.

Schöb, C., Callaway, R. M., Anthelme, F. et al. (2014).The context dependence of beneficiary feedbackeffects on benefactors in plant facilitation. Journal ofPhysiology, 204, 386–96.




www.cambridge.org



Schoener, T. W. (1987). Leaf pubescence in buttonwood:community variation in a putative defense againstdefoliation. Proceedings of the National Academy of Sci-

ences, 84, 7992–5.Schoener, T. W., (1988). Leaf damage in island button-wood, Conocarpus erectus: correlations with pubes-cence, island area, isolation and the distribution ofmajor carnivores. Oikos, 53, 253–66.

Silliman, B. R., Schrack, E., He, Q. et al. (2015). Facilita-tion shifts paradigms and can amplify coastal restor-ation efforts. Proceedings of the National Academy of

Sciences, 112, 201515297.Singer, F. (2016). Ecology in Action. Cambridge UniversityPress, Cambridge.

Skov, M. W. and Hartnoll, R. G. (2002). Paradoxicalselective feeding on a low-nutrient diet: why do man-grove crabs eat leaves? Oecologia, 131, 1–7.

Smith, N. F., Wilcox, C. and Lessmann, J. M. (2009).Fiddler crab burrowing affects growth and produc-tion of the white mangrove (Laguncularia racemosa) ina restored Florida coastal marsh. Marine Biology, 156,2255–66.

Smith, T. J. I., Boto, K. G., Frusher, S. D. and Giddins, R.L. (1991). Keystone species and mangrove forestdynamics: the influence of burrowing by crabs onsoil nutrient status and forest productivity. EstuarineCoastal And Shelf Science, 33, 419–32.

Smith, T. J. I. (1992). Forest Stucture. InA. I. Robertson andD. M. Alongi, eds. Tropical Mangrove Ecosystems. Ameri-can Geophysical Union, Washington, DC, pp. 101–36.

Sousa, W. P. and Dangremond, E. M. (2011). Trophicinteractions in coastal and estuarine mangrove forestecosystems. Treatise on Estuarine and Coastal Science, 6,43–93.

Stieglitz, T., Clark, J. F. and Hancock, G. J. (2013). Themangrove pump: the tidal flushing of animalburrows in a tropical mangrove forest determined

from radionuclide budgets. Geochimica et Cosmochi-

mica Acta, 102, 12–22.Tamooh, F., Huxham, M., Karachi, M., Mencuccini, M.,Kairo, J. G. and Kirui, B. (2008). Below-ground rootyield and distribution in natural and replanted man-grove forests at Gazi bay, Kenya. Forest Ecology and

Management, 256, 1290–7.Tahvanainen, J. O. and Root, R. B. (1972). The influenceof vegetational diversity on the population ecology ofa specialized herbivore, Phyllotreta cruciferae (Coleop-tera: Chrysomelidae). Oecologia, 10, 321–46.

Thampanya, U., Vermaat, J. E. and Duarte, C. M. (2002).Colonization success of common Thai mangrovespecies as a function of shelter from water move-ment. Marine Ecology Progress Series, 237, 111–20.

Thampanya, U., Vermaat, J. E., Sinsakul, S. and Panapi-tukkul, N. (2006). Coastal erosion and mangrove pro-gradation of Southern Thailand. Estuarine, Coastal andShelf Science, 68, 75–85.

Van Mele, P. (2008). A historical review of research onthe weaver ant Oecophylla in biological control. Agri-cultural and Forest Entomology, 10, 13–22.

Vogt, J., Lin, Y., Pranchai, A., Frohberg, P., Mehlig, U.and Berger, U. (2014). The importance of conspecificfacilitation during recruitment and regeneration: acase study in degraded mangroves. Basic and Applied

Ecology, 15, 651–60.Walker, B. and Salt, D. (2012). Resilience Thinking: Sus-

taining Ecosystems and People in a Changing World.Island Press, Washington, DC.

Wilson, J. B. and Agnew, A.D.Q. (1992). Positive-feed-back switches in plant communities. Advances in Eco-

logical Research, 23, 263–336.Winterwerp, J. C., Borst, W. G. and de Vries, M. B.(2005). Pilot study on the erosion and rehabilitationof a mangrove mud coast. Journal of Coastal Research,212, 223–30.




www.cambridge.org

facilitation in mangrove ecosystems - aces · mangrove trees. we begin with the initial...

Documents