ANRV399-MA02-15 ARI 9 November 2009 16:7

Biocomplexity in
Mangrove Ecosystems
ANNUAL
REVIEWS Further I.C. Feller,1 C.E. Lovelock,2 U. Berger,3 K.L. McKee,4
Click here for quick links to
Annual Reviews content online, S.B. Joye,5 and M.C. Ball6
including:
1
• Other articles in this volume Smithsonian Environmental Research Center, Smithsonian Institution, Edgewater,
• Top cited articles Maryland 21037; email: felleri@si.edu
• Top downloaded articles 2
Centre for Marine Studies and School of Biological Sciences, University of Queensland,
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• Our comprehensive search St. Lucia, QLD 4072, Australia; email: c.lovelock@uq.edu.au
3
Institute of Forest Growth and Computer Science, Dresden University of Technology,
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01737 Tharandt, Germany; email: uta.berger@forst.tu-dresden.de

4
U.S. Geological Survey-National Wetlands Research Center, Lafayette, Louisiana 70506;
email: mckeek@usgs.gov
5
Department of Marine Sciences, University of Georgia, Athens, Georgia 30602-3636;
email: mjoye@uga.edu
6
Research School of Biological Sciences, Australian National University, Canberra ACT 0200,
Australia; email: marilyn.ball@anu.edu.au

Annu. Rev. Mar. Sci. 2010. 2:395–417 Key Words

First published online as a Review in Advance on emergent properties, collective properties, trait plasticity, habitat stability,
October 9, 2009
nutrient cycling, individual-based models
The Annual Review of Marine Science is online at
marine.annualreviews.org Abstract
This article’s doi: Mangroves are an ecological assemblage of trees and shrubs adapted to grow
10.1146/annurev.marine.010908.163809
in intertidal environments along tropical coasts. Despite repeated demon-
Copyright  c 2010 by Annual Reviews. stration of their economic and societal value, more than 50% of the world’s
All rights reserved
mangroves have been destroyed, 35% in the past two decades to aquacul-
1941-1405/10/0115-0395$20.00 ture and coastal development, altered hydrology, sea-level rise, and nutri-
ent overenrichment. Variations in the structure and function of mangrove
ecosystems have generally been described solely on the basis of a hierarchical
classification of the physical characteristics of the intertidal environment, in-
cluding climate, geomorphology, topography, and hydrology. Here, we use
the concept of emergent properties at multiple levels within a hierarchical
framework to review how the interplay between specialized adaptations and
extreme trait plasticity that characterizes mangroves and intertidal environ-
ments gives rise to the biocomplexity that distinguishes mangrove ecosys-
tems. The traits that allow mangroves to tolerate variable salinity, flooding,
and nutrient availability influence ecosystem processes and ultimately the
services they provide. We conclude that an integrated research strategy using
emergent properties in empirical and theoretical studies provides a holistic
approach for understanding and managing mangrove ecosystems.

395
 ANRV399-MA02-15 ARI 9 November 2009 16:7

INTRODUCTION
Mangrove ecosystems are coastal wetlands dominated by woody plants that span gradients in
latitude (30◦ N to 37◦ S), tidal height (<1 m to >4 m), geomorphology (oceanic islands to riverine
systems), sedimentary environment (peat to alluvial), climate (warm temperate to both arid and
wet tropics), and nutrient availability (oligotrophic to eutrophic). Across this spectrum, mangrove
ecosystems are critical not only for sustaining biodiversity but also because of their direct and
indirect benefits to human activities (Walters et al. 2008, Koch et al. 2009). Yet, at least 35% of the
world’s mangrove forests have been lost in the past two decades (Valiela et al. 2001, Alongi 2002),
which directly affects ecosystem services such as habitat for fish, prawns, and crabs (Aburto-
Oropeza et al. 2008). Additionally, degradation of the remaining mangrove habitats results in
loss of ecological functionality, putting millions of coastal people in jeopardy. Understanding the
immense complexity of the interacting processes that determine and maintain biodiversity and
productivity of mangrove ecosystems is a major challenge.
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HIERARCHICAL APPROACHES TO MANGROVE ECOLOGY

Mangroves have been the subject of some of the earliest attempts to model the function of coastal
ecosystems via energy and material flux (Odum & Heald 1975). From these inspiring early models,
work on the function of mangroves has expanded to other sites and has revealed a high level of
variability in many aspects of these ecosystems (Robertson & Alongi 1992). As researchers have
tried to evaluate variation in these ecosystems, hierarchical schemes have been developed. Some of
the most successful are based on the geomorphological models by Thom (1982), which were im-
proved by Semeniuk (1985) and Woodroffe (1992). More recently, ecohydrology models (Twilley
& Rivera-Monroy 2005) are based on an overarching influence of climatic and geomorphological
features on mangrove forests, which are then modified by factors lower in the hierarchy and at
smaller spatial scales of topography and hydrology, giving rise to characteristic mangrove and
associated vegetation.
A hierarchical scheme based on physical characteristics (geomorphology, topography, hydrol-
ogy) has been recommended for use in restoring mangrove forests (Rivera-Monroy et al. 2004,
Krauss et al. 2008), approximating the value of ecosystem services (Ewel et al. 1998) and assessing
the vulnerability to climate change, particularly sea-level rise (Lovelock & Ellison 2007, Gilman
et al. 2008). Although climatic, geomorphological, topographic, and hydrological classifications
are attractive for their simplicity, it is unclear whether these models are sufficient to describe
ecological function within mangroves. For example, the trees that form mangrove ecosystems are
doubtless the foundation species (Ellison et al. 2005), but hydroperiod and competition for lim-
ited resources have profound effects on their growth and community structure (Rivera-Monroy
et al. 2004). Such tree-level interactions cause a cascade of spatiotemporal patterns (e.g., species
zonation), which emerge at higher hierarchical levels of the ecosystem but, in turn, affect the
interactions and traits of the abiotic components and organisms at lower levels.
Individual-based models (IBMs), which explicitly address the traits and interactions of organ-
isms and their environment, have been less well explored than higher-level geomorphological
models. However, IBMs provide new opportunities for understanding the biocomplexity of man-
groves (Berger et al. 2008) (see sidebar, Biocomplexity, below). In this review, our aim is to evaluate
the interplay between processes occurring at different levels in the hierarchy. We use the concept
of emergent properties to explore and highlight characteristics of mangrove ecosystems that arise
from interactions among ecosystem components at different levels/scales and are manifested in
different spatiotemporal patterns. Such traits are frequently described in empirical studies but are

396 Feller et al.

 ANRV399-MA02-15 ARI 9 November 2009 16:7

BIOCOMPLEXITY

The term biocomplexity, a fusion of biological and complexity, was coined by Colwell (1998) in a research initiative
at the National Science Foundation. Biocomplexity is concerned with the complex interrelationships among all
ecosystem components, including human societies. Moreover, these interrelationships may span multiple scales
in space and time and include nonlinear behavior (Ascher 2001). A unique aspect of biocomplexity research is its
emphasis on emergent properties—those properties that arise from a system’s components acting in concert and
may not be readily identified or understood by the study of those components in isolation. The study of biocom-
plexity may lead to improved understanding of global phenomena and to better ways for humans to interact with
the environment. Biocomplexity research takes a holistic approach, requires multidisciplinary teams working at
different scales of inquiry, and produces data that are robust when applied to real-world situations. As a case study,
the Mangrove Biocomplexity project, funded by the National Science Foundation’s Biocomplexity in the Environ-
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ment program, brought together a multidisciplinary team of scientists to study microbial and nutrient controls on
mangrove ecosystems (Feller & Venable 2005). The study’s focal site was located in a mangrove archipelago (Twin
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Cays) in the Mesoamerican Barrier Reef Complex off the coast of Belize.

seldom used for decoding the underlying ecological processes. Scientists working on complexity
theory and complex adaptive systems still debate the exact meaning of emergence and emergent
properties, but for our purpose, only a general definition is needed. Emergent properties (see
sidebar, Emergent Properties and Complex Systems, below) (Figure 1) are patterns or processes
that occur at multiple hierarchical levels within ecosystems. They emerge from traits of system
components and their interactions (Breckling et al. 2006). This approach allows us to expand our
understanding beyond ecogeomorphologic models, which reduce interactions to the exchange of
energy and matter, and IBMs, which usually address the level of organisms but frequently ignore
their embedding within lower and higher hierarchical levels. Additionally, the emergent-property
framework has potential use in the management of ecosystems (Nielsen & Müller 2000) and in
understanding coupled human-natural systems (Liu et al. 2007).

EMERGENT PROPERTIES AND COMPLEX SYSTEMS

The term emergence is central to theories of complex systems. Whereas the concept that “the whole is greater
than the sum of its parts” has been in use since Aristotle, interest in analyzing emergent structures and properties
has flourished during the past decades and is tied to the research on complexity, complex adaptive systems, and
self-organization. Three criteria define emergent properties (Nielsen & Müller 2000, Grimm & Railsback 2005)
as we use this term (Figure 1):
1. Emergent properties are not simply the sum of the properties of the components; rather, they represent a
new quality that derives from the properties and interactions of the components.
2. Emergent properties are of a type different from the properties of the components.
3. Emergent properties cannot be easily predicted from individual components.
The latter does not mean that the emergent behavior of a system is always nebulous, impossible to understand, and
uncertain. In fact, one of the major goals of complexity research and individual-based ecology (Grimm & Railsback
2005) is to understand how properties of ecological systems emerge from the traits and interactions of individuals
and their environment.

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 ANRV399-MA02-15 ARI 9 November 2009 16:7

External Integration level of the forest

influences

Emergent properties
Evaporation pattern of forest canopies
Species zonation pattern
Integration level of the Recruitment pattern
individual trees ...

Emergence

Emergent properties Collective properties

Salinity tolerance Canopy openness/roughness
Flooding tolerance Habitat use along inundation gradient
Reproduction strategies Number of produced seeds/propagules
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... ...

Figure 1
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Characteristic patterns and structures appear as emergent properties at higher hierarchical levels that include
basic physiological processes, interactions among organisms, as well as external influences. The emergent
properties of the forest coexist with collective properties that result directly as a consequence of the
properties of related components at lower hierarchical levels.

HIERARCHIES/SCALES OF EMERGENT PROPERTIES

Specializations for Variable Salinity, Flooding, and Nutrient Availability

In the 57 or so species from 21 families that have made the evolutionary leap into mangrove
habitats (Duke 1992, Ricklefs et al. 2006), salinity and flooding tolerances and the ability to persist
in variable habitats emerge as a result of the interactions among biochemical and morphological
traits with environmental factors. Environmental factors that are important to development of
individual trees are those that influence fundamental physiological processes, e.g., temperature,
light, humidity, nutrient availability, CO2 concentration, oxygen, ion and toxin concentrations in
the root zone, wind and wave velocity, and herbivory (Krauss et al. 2008). Many of these factors,
which are strongly affected by human activities in the coastal zone and by climate change, influence
the properties of tissues, individuals, and ecosystem characteristics at higher hierarchical levels
(Chapin 2003, Liu et al. 2007).

Salinity tolerance. Soil salinity is variable in mangrove habitats, depending on the balance be-
tween evaporation, which concentrates salt, and freshwater flushing, which dilutes salt. Although
most mangroves are halophytes that tolerate saline conditions, some species need salt to grow and
complete their life cycle (Ball 2002). Nevertheless, high salinity has negative consequences for
metabolic processes and growth rates (Ball 1988), and it limits the height and productivity of trees
(Cintrón et al. 1978).
Salinity tolerance requires that halophytes, including mangroves, maintain sufficient freshwater
inside their cells and tissues to maintain metabolic function against a higher osmotic pressure in
the exterior root environment, which can vary between freshwater and three-times seawater salt
concentration. The mechanism by which salinity tolerance is achieved is complex and controlled
by a plethora of genes (Flowers & Colmer 2008, Munns & Tester 2008). In halophytes, some of
the most commonly identified metabolic traits leading to salinity tolerance include the capacity to
(a) control the uptake of Na+ and Cl− ions; (b) isolate salt from sensitive organelles, store Na+ and

398 Feller et al.

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Cl− ions, and excrete the salt in some species (salt glands); and (c) produce high concentrations of
osmotically compatible solutes (Lovelock & Ball 2002, Flowers & Colmer 2008).
In addition to adaptations for ion management in tissues, salinity tolerance also encompasses
physiological and morphological traits that strongly influence ecosystem processes (Ball 1988,
Lovelock & Ball 2002). The ability of halophytes to achieve and maintain high rates of photo-
synthesis under saline soil conditions is linked to higher water-use efficiency than that found in
nonhalophytes (Ball & Farquhar 1984, Clough & Sim 1989). High water-use efficiency is achieved
and safely sustained by a range of traits, which vary among species and influence ecosystem function
at higher scales. These traits include the following:
1. a specialized stomatal anatomy that limits water loss (Tomlinson 1986);
2. high levels of protection from photooxidative damage (Lovelock et al. 1992, Cheeseman
1997);
3. modifications and arrangement of leaves to improve leaf energy balance, in which leaves
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are often smaller and thicker and have upright orientations that avoid direct sun exposure,
thus minimizing transpiration per unit of carbon uptake and maximizing heat loss (Ball et al.
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1988, Lovelock et al. 1992);

4. hydraulic architecture that minimizes the risks of embolism under water-limited conditions
(Lovelock et al. 2006a, Stuart et al. 2007), which is associated with small vessels and dense
wood (Verheyden et al. 2005, Schmitz et al. 2006); and
5. greater carbon investment in roots than leaves (Ball 1988, López-Hoffman et al. 2007)
and deployment of roots into soil-water resources that are more favorable for physiological
function (Greaver & Sternberg 2006, Lambs et al. 2008).
The traits associated with salinity tolerance give rise to mangrove forest canopies that have distinc-
tive energy signatures (Souza-Filho et al. 2006). For example, thick, tough, low-nutrient tissues
and hard wood lead to lower rates of decomposition (Middleton & McKee 2001), herbivory, and
nutrient cycling (Feller et al. 2009).
Salinity tolerance incurs costs that influence ecological processes. High respiratory costs in-
volved in salt uptake and storage (Burchett et al. 1989) influence recruitment and understory
development (López-Hoffman et al. 2007). Despite high concentrations of salt and ammonium
(and other ions) in mangrove soils, root respiration is low compared with that of terrestrial trees
(Burchett et al. 1989) and is highly efficient with respect to nitrogen and phosphorus investment
(Lovelock et al. 2006b). Low nutrient-use-efficient respiratory rates compared with those of many
plant species are likely due to adaptations in root ion-uptake processes that are not understood
(Malagoli et al. 2008) but have flow-on effects on carbon and nutrient cycling at the ecosystem level.

Flooding tolerance. Emerging from a collection of morphological and physiological traits, flood-
ing tolerance is the basis of some of the most valued ecosystem services provided by mangrove
forests. Flooding usually decreases plant growth as it reduces O2 concentrations at the root sur-
face, inhibiting water uptake and other primary physiological functions (Gibbs & Greenway 2003).
Flooding tolerance influences processes ranging from individual growth to community and land-
scape development. Traits that contribute to flooding tolerance include aerial root systems and
aerenchyma (Scholander et al. 1962). Differential flooding tolerance among mangrove species is
linked to variations in root morphologies and physiology (Naidoo 1985, He et al. 2007), which in
turn strongly influence growth and recruitment (Youssef & Saenger 1998) and vegetation patterns
along hydrologic gradients (Smith 1992).
Aerial roots strongly influence the emergent properties of mangrove ecosystems, their function,
and the services they provide. Aboveground roots and stems influence flow rates of tidal waters,

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determining particle-settling rates and sediment retention in mangroves (Wolanski et al. 1992).
Sedimentation is an extremely important process in coastal wetlands, determining nutrient inputs,
productivity, and surface accretion, which in turn influence mangrove forest interactions with
nearshore habitats as well as mangrove responses to sea-level rises and intense storms (Krauss
et al. 2003, Day et al. 2008).

Reproductive traits and regeneration. Many mangroves have evolved a specialized reproduc-
tive strategy in which seeds lack dormancy and are viviparous, germinating precociously while
still attached to the parent plant. These seedlings are buoyant, photosynthetically competent, and
transported in tidal (Rabinowitz 1978, Stieglitz & Ridd 2001) and ocean currents, often over long
distances (Nettel & Dodd 2007). Vivipary is found in many of the most salt- and flood-tolerant
mangrove families (i.e., Rhizophoraceae, Avicenniaceae, Myrsinaceae, Plumbaginaceae, Pellice-
riaceae, Aracaceae) and is associated with low levels of abscisic acid within the embryonic tissues
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(Farnsworth & Farrant 1998).

Vivipary and the buoyancy of seeds and propagules influence processes that are observed at a
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range of scales. Patterns in mangrove vegetation (zonation) were long thought to be due to the
differential movement of propagules of various sizes with tidal movements (Rabinowitz 1978).
Although little experimental support has been found for the propagule-sorting hypothesis (Sousa
et al. 2007), seasonality in reproductive output (Duke 1990) and tidal movement of propagules
upstream has been observed at a rate of 3.2 km/day. This movement is driven by seasonal salinity
gradients and turbulence in creeks (Stiegliz & Ridd 2001), indicating that patterns in recruit-
ment and vegetation may emerge from complex interactions among propagule characteristics,
phenology, and climatic factors.
The production of viviparous propagules is a risky strategy, potentially sustaining high costs
that may have influenced the evolution of other traits. Because of a lack of seed dormancy, forests
affected by large-scale disturbances (hurricanes, tsunamis) may not have local seed reserves, ne-
cessitating reseeding from other sites less impacted by disturbance and requiring long-distance
dispersal in water and longevity of propagules (Nettel & Dodd 2007). Other costs of vivipary
may include a large investment in propagules versus investment in seeds in nonmangrove species.
For example, Bunt (1995) reported the proportion of litterfall that is reproductive material varies
between 4% and 50% of annual litterfall for mangroves at a range of sites around Australia,
whereas for terrestrial tropical forests, the proportional contribution of reproductive material in
litter ranges from 0.4% to 13.1% (Green 1998).
Regeneration of forests after small-scale (gap formation; Duke 2001) or large-scale (hurricanes;
Cahoon et al. 2003) disturbances is dependent not only on seedling recruitment but also on
resprouting of damaged trees (Baldwin et al. 2001). The capacity to resprout or coppice after
disturbances varies among mangrove species. Species in the Avicenniaceae resprout from epicormic
buds, but this does not occur in species in the Rhizophoraceae, making Rhizophoraeae forests
particularly vulnerable to hurricanes (Baldwin et al. 2001, Cahoon et al. 2003), cyclones, frosts
(Lugo & Patterson-Zucca 1977, Smith et al. 1994), and sediment deposition from storms or
human activities (Ellison 1998). Both the impacts of disturbance on mangrove forests and their
recovery from disturbances can depend on the dominant species, phenology, and the distribution
and longevity of reproductive individuals.

Nutrient availability. Soil nutrient availability is variable within and among mangrove ecosys-
tems, ranging from extremely low in oceanic settings to very high in accreting muddy systems
and those receiving effluent from rookeries, aquaculture, and human developments (Alongi 2009).
It can vary spatially along tidal gradients and temporally with seasonal and interannual variation

400 Feller et al.

 ANRV399-MA02-15 ARI 9 November 2009 16:7

in nutrient delivery and cycling. From fertilization experiments over a range of sites, it has been
established that tree growth is nutrient limited in many mangrove forests (Lovelock et al. 2007,
Naidoo 2009).
Many mangrove species have traits that give rise to efficient nutrient use and conservation when
challenged by nutrient limitations (Feller et al. 2009). High nutrient-use efficiency (NUE) and
variation in NUE in mangrove species emerge from a range of physiological and morphological
traits, including enhanced investment in roots relative to shoots (Naidoo 2009); long leaf life spans
(Duke 1990, Suárez 2003); high resorption efficiencies in tissues prior to senescence (Feller et al.
2009); thick, sclerophyllous leaves (Feller & Chamberlain 2007); low leaching losses (Wanek et al.
2007); high photosynthetic NUE (Lovelock & Feller 2003, Martin 2007); and NUE of root and
other metabolic processes (Lovelock et al. 2006c).
Plant traits that confer tolerance of low nutrient availability have strong effects on ecosystem
processes (Chapin 2003) and contribute to the emergent properties of mangrove ecosystems
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at greater spatial and temporal scales (Feller et al. 2009). Two neotropical species observed to
be highly adapted to low nutrient availability are Rhizophora mangle and Laguncularia racemosa.
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Respiration and photosynthesis per unit tissue nutrient are high in these species compared with
their competitor Avicennia germinans (Lovelock et al. 2006a, 2006b). Additionally, investment in
roots, tissue nutrient concentrations, and sclerophylly and chemical defenses are also enhanced
in R. mangle and L. racemosa relative to A. germinans (McKee 1995). These species differences
in traits related to nutrient conservation influence resistance to herbivores and pathogens (Feller
1995, Feller & Chamberlain 2007), decomposition of tissues (Middleton & McKee 2001), and
surface elevation gains (Krauss et al. 2003). Differences in NUEs may also contribute to patterns
of species distribution over salinity, hydrologic, and nutrient gradients (Berger et al. 2006), which
in turn alter productivity (Saenger & Snedaker 1993), responses to disturbance, and patterns of
succession (Sherman et al. 1998, Piou et al. 2006).

Trait Plasticity
High levels of plasticity in plant traits arise and are maintained in populations when environments
are variable, environmental cues are reliable, and specialization has costs (Callaway et al. 2003).
Mangroves display a high level of trait plasticity in response to salinity, flooding, and nutrient
availability. For example, growth and metabolism of many mangrove species decline when salt
is withheld (Ball 2002), suggesting a loss of competitive ability under “terrestrial” conditions.
Growth of mangroves is also slowed under hypersaline conditions, but many species can maintain
some level of growth (e.g., dwarf or scrub forms), albeit at a very slow rate, under extremely
adverse conditions (Feller 1995, Lovelock et al. 2005). Species that form dwarf or scrub forest
stands are often capable of attaining very high growth rates that match those of terrestrial forests
(Dadhouh-Guebas et al. 2004, Feller et al. 2009). Mature tree size for the neotropical species
R. mangle varies between 0.5 and 40 m (Lugo 1997, Golley et al. 1975). The coefficient of variation
of hydraulic conductivity (which can be used as a measure of trait plasticity) of R. mangle stems is
0.2 greater than the variation in nutrient availability. By way of contrast, the mean coefficient of
variation of hydraulic conductivity among 17 different species of oaks is 0.12 (Cavender-Bares et al.
2004). These and other examples of trait plasticity (McKee et al. 2007b, Feller & Chamberlain
2007) suggest that mangrove species are highly plastic in comparison to many terrestrial species.
On an ecosystem level, high levels of trait plasticity yield forests that can vary widely in structure
and age but are comprised of one species (Dadhouh-Guebas et al. 2004, Lovelock et al. 2005). Even
though studies of competition and facilitation among mangrove tree species are rare, the range
in plasticity among mangrove tree species in response to salinity (Ball 1996), nutrient availability

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 ANRV399-MA02-15 ARI 9 November 2009 16:7

(Lovelock & Feller 2003), flooding, and climate (Cardona-Olarte et al. 2006, He et al. 2007) may
influence community composition and, ultimately, carbon and nutrient cycling in forests.

EMERGENT AND COLLECTIVE PROPERTIES OF FORESTS

Zonation
Landscape-level patterns that emerge in mangrove forests have long captivated scientists, giving
rise to a rich observational and experimental tradition (Krauss et al. 2008). Mangrove forests
are described as having “zones” of vegetation, typically arranged along tidal gradients that are
dominated by one or two species. Although species zones have been represented graphically
(Smith 1992), they have defied statistical detection in species-rich regions, leading Smith (1992),
Bunt & Stiegliz (1999), and Ellison et al. (2000) to conclude either that environmental gradients
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and their effects on species performances are very complex or that dispersal and recruitment are
random.
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Ecophysiological studies have revealed that many species may co-occur because of similar
physiological requirements (Ball 1996) and that strong patterning in vegetation emerges on the
extreme ends of environmental gradients (e.g., salinity, flooding, nutrient availability) (Ball 1998).
Thus, abiotic factors are likely to be most important in driving vegetation patterns through their
differential effects on seedling growth and mortality in unfavorable environments (Ball 1996).
In more favorable settings, competition or facilitation among species may also be important in
determining zonation. Different species may modify environments sufficiently to affect competi-
tors either above- or belowground (Passioura et al. 1992). Variations in species salinity tolerance
(Ball 1996), shade tolerance (Lovelock et al. 1992, López-Hoffman et al. 2007), flood tolerance
(Cardona-Olarte et al. 2006, He et al. 2007), and nutrient requirements (Lovelock & Feller 2003)
may all have a role, although there are few experimental tests of direct competition (Smith 1992).
Experimental studies have also indicated an important role for biological agents, with particular
emphasis on seedling predators (crabs and beetles) (Smith 1987, Sousa et al. 2007).
Tree species zonation, or at least differential tree species distributions, within the intertidal
zone have wide-ranging effects on the properties of mangrove ecosystems that depend on the
traits of species and their interactions with the environment (Chapin 2003). Differences among
species in root structure, stem densities, and canopy characteristics influence material exchange
during tidal flow, atmospheric exchange, as well as ecosystem responses to disturbances (Cahoon
et al. 2003, Koch et al. 2009) and sea-level rise (McKee et al. 2007a). The variable effects of human
exploitation and activities on mangrove forests are also heavily dependent on species distributions
(Dahdouh-Guebas et al. 2005, Alongi 2009).

Productivity
The productivity of mangrove forests is important for supporting mangrove and adjacent coastal
food webs and for the stability of mangrove-fringed coasts. The productivity of mangrove forests
can be equivalent to the most productive terrestrial forests, although it is highly variable over
both large (latitudinal) and smaller (hydrological) scales (Bouillon et al. 2008, Alongi 2009). For
example, in nutrient-rich riverine systems or the bird rookeries of the Neotropics, Rhizophora
trees grow to more than 40 m tall and are highly productive (Golley et al. 1975). However, behind
tall fringing forests or in nutrient-poor areas on offshore islands, old-growth forests at many sites
are dominated by stunted stands with low productivity, ≤1.5 m tall (Lugo 1997). Variation in the
primary productivity of mangrove forests emerges from a wide range of biotic and abiotic factors

402 Feller et al.

 ANRV399-MA02-15 ARI 9 November 2009 16:7

and results in highly variable environments for seedlings and other plants and fauna. Interactions
among productivity, geomorphology, and hydrology influence material exchange with tidal waters
via outwelling and inwelling, thus also impacting the services provided by mangrove ecosystems
within larger and connected coastal ecosystems (Alongi 2009).
Net primary productivity (NPP) of forests is determined by the balance of the total CO2 fixed
by the forest (gross primary productivity) and total plant respiration, suggesting NPP can be
considered a collective property of ecosystems. Gross primary productivity in mangrove forests,
like that of terrestrial forests, is often estimated with simple algorithms using leaf area index (leaf
area per unit ground area), light attenuation, or photosynthetic rates (Alongi 2009). The respiratory
components of mangrove forests are poorly parameterized, though rates of CO2 release from trees
are substantial and dominated by the woody parts and roots (Lovelock 2008, Alongi 2009). The
contribution of soil microbial processes in current carbon budgets of mangrove ecosystems is
likely to be underestimated. Mineralization of sediments (imported), organic matter (particularly
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fine roots), and microbially derived organic matter may also be important in some areas, with
these processes possibly leading to substantial carbon exports from porewater to coastal waters
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(Alongi 2009, Bouillon et al. 2008). Additional research is needed to better constrain the rates of
and controls on soil respiration so that the fates of mangrove-derived and other organic matter
within mangrove forests can be determined.
In mangrove forests, as in other forests, NPP has usually been estimated by leaf litterfall, but
litterfall may represent only ∼25–30% of mangrove forest NPP. Thus, NPP has been generally
underestimated (Bouillon et al. 2008, Alongi 2009). Increments in accumulated wood and roots
and losses of roots and other tissues as well as root exudates have been measured less frequently
but may account for up to 70% of NPP. Variations among the components that comprise NPP
among forests over environmental gradients are likely to influence ecosystem function, particularly
affecting processes that link mangroves to adjacent ecosystems.
Other primary producers in mangrove ecosystems that are not usually considered in NPP
include phytoplankton in tidal waters, benthic cyanobacterial and microalgal mats, algal turfs, and
the distinctive root epiphytic algal community (the Bostrychietum) that adheres to aboveground
roots and stems. These components may be more important than their absolute contribution
to NPP because they may be preferentially decomposed and consumed (Bouillon et al. 2008).
Benthic cyanobacterial and microalgal mats are common in scrub forests where high light levels
reach the benthos. In these habitats, the mats may be as or more productive than the trees. These
mats also play key roles in nutrient cycling (Lee & Joye 2006). The epiphytic algal community is
also highly productive, contributing up to 15% of forest gross primary productivity (Dawes et al.
1999). In addition to providing tissue that is more palatable to consumers than mangrove leaves,
the epiphytic algal community increases frictional resistance, which affects flow rates of the water
and deposition of sediment, nutrients, and organic matter within the mangroves (Wolanski et al.
1992).

Nutrient and Carbon Cycling

The biogeochemical signature of mangroves and other coastal wetlands is a collective property
stemming from the biological, physical, and chemical interactions among flood- and salt-tolerant
plants and microbial processes in soils. Mangrove forests are intensely affected by a tidally mediated
exchange of materials. Tides connect the mangrove fringe and the nearshore waters, whereas
interior forests are more isolated in the landscape. The fringe is an open system, often accumulating
subsidies of sediments as well as wrack (Wolanski et al. 1992) and nekton (Sheaves 2005), while
exporting particulate and dissolved organic matter via tidal exchange ( Jennerjahn & Ittekkot

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 ANRV399-MA02-15 ARI 9 November 2009 16:7

2002). Interior habitats, which are often dominated by scrub forests, are closed systems with a
more pulsed materials exchange. Differing degrees of “openness” between fringe and interior
habitats impact their nutrient stoichiometry (Kristensen et al. 2008).
Allocthonous subsidies (e.g., seagrass wrack, polysaccharide-bound particulates, nekton waste
products) to mangrove fringes have low C:P and C:N values (Ayukai & Wolanski 1997), compared
with outwelled materials of mangrove origin, which have higher C:N:P ratios (Bouillon et al. 2008).
Scrub forests, ponds, and microbial mats export substantial amounts of dissolved organic nitrogen
and carbon to tidal creeks ( Joye et al. 2005). Nitrogen fixation in microbial mats provides a nutrient
subsidy for scrub mangrove trees, adjacent forests, and benthic and planktonic communities ( Joye
& Lee 2004, Lee & Joye 2006).
Nutrient cycling in mangrove habitats reflects a balance between nutrient inputs, availability,
and internal cycling (Lee et al. 2008). Microbial processes alter soil nutrient concentrations and
nutrient cycling. Denitrification reduces inorganic nitrogen concentrations and could drive nitro-
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gen limitation of plant production ( Joye 2002). In contrast, microbial nitrogen fixation increases
nitrogen inventories and ameliorates nitrogen limitation of plant production ( Joye & Lee 2004).
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Microbial processes affect phosphorus availability indirectly. In addition to mediating nutrient cy-
cling, anaerobic microbial processes oxidize particulate and dissolved organic matter in soils (Lee
et al. 2008). Thus, nutrient availability and cycling are intimately linked to microbially mediated
carbon turnover in mangrove soils.
Inputs of excess nutrients to mangroves can alter patterns of nutrient limitation over time,
but not all ecological processes or ecosystem components exhibit the same pattern of nutrient
limitation (Feller et al. 2009). However, nutrient controls on ecosystem components, such as
benthic microalgae, are poorly described or unknown ( Joye & Lee 2004). Nitrogen enrichment
may increase release of dissolved organic matter from mangrove soils occupied by microbial mats,
as documented in benthic microalgae-dominated salt marsh sediments (Porubsky et al. 2008).
Despite their small areal extent, mangrove forests play an important role in global carbon
cycling. They are responsible for substantial fluxes of dissolved organic carbon (DOC) to the
ocean (Dittmar et al. 2006, Bouillon et al. 2008), accounting for 15% of the carbon stored in
marine sediments and sequestering a global average of 10.7 mol carbon m-2yr-1 of atmospheric
CO2 in peat ( Jennerjahn & Ittekkot 2002). Dittmar et al. (2006) found that 10% of the terrestrially
derived DOC in the oceans is derived from mangroves. Similarly, high fluxes of dissolved organic
nitrogen and DOC from mangrove soils to the overlying waters were documented in Belize and
Panama ( Joye et al. 2005). These fluxes of nutrients and organic material to the ocean are expected
to increase further as a result of mangrove clearing and nutrient enrichment (Bouillon et al. 2008).
Microbial biomass and activity estimates in mangrove soils suggest that most bacteria remain
unconsumed, eventually lysing to support continued bacterial production and release of dissolved
nutrients (Kristensen et al. 2008). Microbial activity in soils and sediments are ultimately con-
trolled by inputs of dissolved and particulate organic matter and may also be limited by nutrient
availability (Sundareshwar et al. 2003). Variation in nutrient versus carbon limitation of microbial
decomposition in mangroves may contribute to differences in carbon-recycling efficiencies. Al-
though the flux of DOC from mangroves to the ocean is an important part of the carbon cycle, it
remains poorly understood (Kristensen et al. 2008).
In addition to DOC fluxes via water, carbon accumulations in soils and flux to the atmosphere
via root respiration are also important parts of the carbon cycle (Alongi 2008). In mangrove forests,
fine root production, forest stature, and variations in nutrient availability are likely to be important
factors determining carbon flux (Lovelock et al. 2006c), but soil respiration is similar to terrestrial
systems and is correlated with aboveground production (Lovelock 2008).

404 Feller et al.

 ANRV399-MA02-15 ARI 9 November 2009 16:7

Habitats and Food Webs

A complex community structure distributed vertically through supratidal, intertidal, and subtidal
zones and horizontally across the land-sea ecotone is an emergent property of mangrove forests
that has arisen out of specializations of individual species to the intertidal zone. The structure
provided by these species essentially defines mangrove communities and ecosystems by creating
habitats and stable conditions, modifying abiotic environments, and modulating ecosystem pro-
cesses. Similar to terrestrial trees, mangroves are composed of a woody bole and a leafy canopy
inhabited by ecological communities not unlike those found in other tropical forests. But, unlike
terrestrial species, the aerial root systems of mangroves also form an extensive aboveground struc-
tural framework, which dramatically increases the architectural complexity of these forests. These
structures not only provide habitat for supratidal and intertidal communities, but they also often
suspend into the adjacent water column where they are colonized by rich assemblages of organisms
and provide food and shelter for fish, shrimp, and other nektonic organisms (Nagelkerken et al.
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2008). Because mangroves are typically mud- or peat-based systems, prop roots provide the hard
substrate essential for settlement by many sessile marine organisms.
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Species diversity, as a collective property of mangrove ecosystems, stems directly from the
spectrum of habitats created and modified by these trees. Despite low species richness of mangrove
vegetation, recent reviews (Cannicci et al. 2008, Krauss et al. 2008, Nagelkerken et al. 2008) have
summarized an extensive body of literature documenting the habitat function of mangroves and
the impacts of the fauna on forest development, productivity, and structural complexity. In the
supratidal, the mangrove canopy supports a terrestrial fauna that, like other forests, is dominated
by insects but also includes birds, mammals, lizards, snakes, snails, crabs, and spiders. In the
Neotropics, the diversity of vertebrates associated with mangroves is low with few endemic species.
That situation is different in Australian mangrove communities, where there are many endemic
species, especially birds (Luther & Greenberg 2009). Biogeographic studies indicate that most
species are a subset of the terrestrial fauna and disperse into the mangrove by swimming, flying,
or rafting inside or on pieces of wood or other floating debris (Rützler & Feller 1996, Brooks &
Bell 2001).
Mangrove forests have been described as detritus-based ecosystems where primary consumers
play a minor role (Tomlinson 1986). However, recent studies have shown that herbivory in man-
groves is comparable to that of other temperate and tropical forests (Cannicci et al. 2008). Similar
to their role in other ecosystems, mangrove herbivores play important ecological roles that include
decreasing primary production, increasing habitat and community complexity, creating light gaps,
interfering with internal nutrient cycling, and increasing nutrient losses (Feller 2002). This fauna
is characterized by specialized, cryptic, endophytic species, that are comprised of miners, gallers,
and borers (Feller & Chamberlain, 2007, Feller et al. 2007). In the intertidal, typical substrates
for benthic organisms include tree trunks, aerial roots, peat banks, and mud- and saltflats. Here,
alternating submergence and exposure and fluctuating salinity create stressful environmental con-
ditions. Whereas the mangrove understory is noted for its lack of diversity of vascular flora, the
intertidal portions of aerial roots support a diverse intertidal assemblage of algal epiphytes, which
in turn host a variety of invertebrates (Kieckbusch et al. 2004, Lee 2008). Algal mats on the soil
surface are also home to numerous taxa of marine invertebrates (Kathiresan & Bingham 2001).
Mangrove mud- and saltflats are often covered in thick, laminated cyanobacterial mats that pro-
vide habitat and food resources for many benthic organisms, including invertebrates, amphibious
fish, and sea snakes (Cannicci et al. 2008). The biocomplexity of mangrove communities is fur-
ther enhanced by organisms (crabs, fish, birds, and mammals) that migrate across tidal zones and
thereby link supratidal, intertidal, and subtidal food webs (Vannini et al. 2008).

www.annualreviews.org • Biocomplexity in Mangrove Ecosystems 405

 ANRV399-MA02-15 ARI 9 November 2009 16:7

Although mangrove productivity is highest in coastal and riverine forests, most species are
found in the associated subtidal habitats. The subtidal communities of coastal mangroves are less
diverse than in offshore mangrove islands where the water is clear and more reef-like (Rützler
& Feller 1996). In those areas, aerial roots provide structure for a dense assemblage and colorful
array of sessile epibionts, including algae, sponges, tunicates, and anemones, and support diverse
ecological interactions between mangroves and these subtidal epibionts, ranging from mutualistic
to parasitic.

EMERGENT PROPERTIES OF ECOSYSTEMS AND LANDSCAPES

Habitat Stability
Even though coastal systems are subject to changing sea levels, hurricanes, and tsunamis (Alongi
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2008), many mangrove habitats sustain themselves for millennia (Gilman et al. 2008). For example,
mangrove islands in the Mesoamerican Barrier Reef system of Belize have existed for ∼8000 years
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and have accumulated more than 10 m of peat as sea level has risen (Macintyre et al. 2004).
Vertical building of these islands has allowed them to maintain surface elevations within the
intertidal (Figure 2), where mangroves have dominated for their entire history (McKee & Faulkner
2000, McKee et al. 2007a). Thus, an emergent property of these biogenic mangrove systems is
habitat stability, which is defined here as persistence of the mangrove habitat, relatively unchanged,
through time.
Stability of mangrove habitats arises from the interaction of physical, chemical, and biological
components operating at different spatial, temporal, and organizational scales. Processes occurring
at the cellular, organism, population, ecosystem, and landscape scales contribute to habitat stability.
Any disturbance that alters these processes may cause the system to collapse or to convert to some
other habitat, for example, where mangroves have invaded and converted a saltmarsh (Rogers et al.
2006). If sea-level rise exceeds the capacity of a mangrove system to build vertically, it will become
a subtidal system, as is predicted for low-lying oceanic islands. Conversely, if elevation gain raises
the mangrove surface above the intertidal, the system may be invaded by upland vegetation. How-
ever, the latter is unlikely to occur without exogenous input of sediments. As elevation changes,
flooding depth and duration influence plant production and decomposition. This feedback pro-
cess allows the mangrove system to adjust to prevailing water levels and persist through time
(Figure 2).
For a group of mangrove islands in the Caribbean, McKee et al. (2007a) showed that peat is
primarily composed of mangrove roots and that fossil roots, >7000 years old, are indistinguishable
from modern roots. The buildup of peat caused upward expansion of the soil surface at rates
sufficient to keep pace with sea-level rise over the Holocene. As sea-level rise in the Caribbean
slowed ∼2000 to 3000 years bp (before the present) (Toscano & Macintyre 2003), peat formation
slowed. Elevation change on Belizean islands, measured with surface elevation tables from 2000
to 2008, average ∼3.5 mm year−1 (K.L. McKee, unpublished data), which is similar to global
sea-level rise rates (3.4 mm year−1 ; Nerem & Choe 2009). These data support the existence of a
feedback mechanism that allows mangrove systems to adjust to prevailing sea-level conditions. This
feedback likely occurs through the change in flooding conditions and its effect on sedimentation
and production-decomposition processes as elevations fluctuate during soil formation. In peat
soils with moderate flooding, root production is high and decomposition is slow, leading to peat
formation. As peat accumulates and the soil surface expands upward, there is a decrease in flooding
depth and duration. As flooding decreases, peat formation and sedimentation slows—leading to a
feedback control on vertical land-building.

406 Feller et al.

 ANRV399-MA02-15 ARI 9 November 2009 16:7

Landscape

Habitat stability during

sea-level change
Ecosystem
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Peat formation and

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biogenic land-building

Population

Root system dynamics

of mangrove stands

Holocene sea level rise

(density, depth, turnover)

Organism/species Vertical
accumulation
of peat

“Flood tolerance” of
mangroves
Cell/tissue

Pleistocene limestone
Root metabolic/
anatomical adaptations
to flooding

Figure 2
Biocomplexity of biogenic mangrove forests results in the emergent property of habitat stability, i.e., persistence during sea-level
change via peat formation and vertical land-building. Characteristics of mangroves at different organizational scales generate a capacity
to self-adjust to the prevailing flooding regime. Stress adaptations (metabolic and anatomical) to flooding at the cell or tissue scale lead
to the emergent property of flood tolerance at the organism or species scale. The tolerance of anaerobic conditions allows prolific
production of mangrove roots in flooded soils, but physical limits to root aeration promote root growth at or near the soil surface. As
roots die, their decomposition is retarded owing to lack of oxygen, which promotes peat formation. The buildup of peat causes upward
expansion of the soil surface and a consequent decrease in flooding depth and duration. As flooding stress decreases, peat formation
slows—leading to a feedback control on vertical land-building. The net result of these feedback processes at the landscape scale is the
emergent property of habitat stability. In some cases, mangrove forests may persist for millennia unless disturbed in such a way as to
alter the feedback controls on land elevations.

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 ANRV399-MA02-15 ARI 9 November 2009 16:7

Persistence of biogenic mangroves over geological time depends on processes occurring over
shorter intervals, e.g., annual production of plant roots. Spatial variation in mangrove productivity,
tidal fluctuation, nutrient availability, and other factors causes landscape-level variation in habitat
stability. For example, spatial variation in elevation change is associated with different rates of be-
lowground production (McKee et al. 2007a). Thus, habitat stability arises from interrelationships
across spatial, temporal, and organizational dimensions.
When a disturbance causes widespread mortality of biogenic mangroves, the sudden death of
the root system and lack of root production may lead to peat collapse and alter habitat stability, as
occurred in the Bay Islands, Honduras, in 1998 following Hurricane Mitch (Cahoon et al. 2003).
Forests with little damage showed elevation gains (5 mm year−1 ) in concert with high rates of
root production in the years following the hurricane. However, forest stands that suffered near-
total mortality experienced peat collapse (−11 mm year−1 ). Model simulations predicted that peat
collapse would continue for at least eight more years at a rate of 7 mm year−1 in the absence
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of mangrove recovery. Anthropogenic disturbances caused by sediment burial may also lead to
the collapse of mangroves (Ellison 1998). Another growing threat results as mangroves are being
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cleared and filled to support resort development and vegetation typical of the beach habitat. In the
Caribbean, developers are converting offshore mangrove islands into tourist resorts (Macintyre
et al. 2009, McKee & Vervaeke 2009). Here, removal of mangroves and burial of the underly-
ing peat with sediments dredged from the surrounding seafloor have altered soil characteristics,
increased erosion, and reduced the capacity of these islands to keep pace with sea level. Thus,
subsidence of the peat and sea-level rise will submerge such areas, despite temporary increases in
elevation by filling.

Connectivity
Mangroves are connected to both subtidal and terrestrial environments through movement of
water across ecosystem boundaries and through movement of fauna. Mangroves serve not only as
sources of subsidies (carbon and nutrients; Kristensen et al. 2008) and fauna for adjacent environ-
ments (Nagelkerken et al. 2008), but also as sinks in the land-seascape (Bouillon et al. 2008). The
connectivity between mangroves and adjacent ecosystems and food webs (Aburto-Oropeza et al.
2008) is an emergent property that arises out of the interactions among the landscape, geomor-
phology, hydrology, climatic and tidal regimes, structural characteristics, accessibility to fauna,
and the proportion of edge to area of mangrove forests, which enhances the potential for ex-
change across boundaries (Nagelkerken et al. 2008). This connectivity not only contributes to the
economic value placed on mangroves, but also increases their vulnerability to human and natural
disturbances (Alongi 2008).
Exchange of material and fauna in tidal waters has been extensively examined because of the
vital role mangroves play in supporting fisheries (Nagelkerken et al. 2008), their role as filters
where sediments and nutrients are trapped (Alongi 2009), and the recent discovery of the impor-
tance of mangrove-derived carbon to oceanic production through microbial processing (Dittmar
et al. 2006). Although we have a general understanding of the scope of the ecosystem services
provided through tidal connectivity of mangroves and near-shore waters, the factors that deter-
mine variability in the provision of these services are complex and likely nonlinear (Koch et al.
2009). The fisheries value of mangroves depends on a range of factors that include the species
being considered (habitat, ontogenetic stage, feeding preferences); site characteristics (currents,
tidal flow, turbidity, area and arrangement of habitats); climatic variability (diurnal, seasonal, an-
nual, decadal); and presence, abundance, and movements of competitors and predators (Faunce
& Serafy 2006, Aburto-Oropeza et al. 2008). Although mangroves may function as nurseries for

408 Feller et al.

 ANRV399-MA02-15 ARI 9 November 2009 16:7

many species, direct evidence for fish migrations between mangrove and offshore habitats is scarce
(Nagelkerken et al. 2008). For successful integrated management of mangroves, an understand-
ing of the complexity of factors that give rise to productive and diverse fisheries is vital. Marine
protected areas that embrace multiple habitat types and include the terrestrial catchments have
the greatest potential for success (Heyman & Kjerfve 1999).
Less well studied is the connectivity among terrestrial species and mangrove habitats and
fauna. At the landscape scale, mangroves are ecotones where marine and terrestrial food webs
often overlap, where marine organisms gain access to terrestrial prey, and where terrestrial fauna
have access to marine prey or to other terrestrial fauna that visit mangroves for refuge or feeding
(Nagelkerken et al. 2008). The interruption of mangrove-terrestrial ecotones is a common result
of coastal developments, which alter tidal incursions and disrupt exchange across the ecotone with
largely undocumented consequences (Walters et al. 2008).
Connectivity to rivers and tidal water underlies the biofiltration services mangroves provide.
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Variation in the level of sediment retention, which is important for adjacent coral reef and sea-
grass ecosystems requiring high light levels at the benthos, has been attributed to interacting
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factors, which include the following: (a) the friction to tidal fluxes offered by roots and burrows;
(b) the position in the forest (forest edges trap more sediment and particles than do forest interiors);
(c) seasonal variation in the heights and strengths of tidal flows; (d ) variation in sediment loads; and
(e) the geomorphology and hydrology that control riverine flows, currents, and tidal amplitudes
(Wolanski et al. 1992). Nutrient exchange, which facilitates capture and liberation of nutrients
that enhance coastal production, is influenced by spatial and temporal factors as well as factors that
control primary production of trees, macroalgae, microphytobenthos, and microbial communities.
Disruption of connectivity between mangroves and other components of the landscape can have
negative consequences. Loss of mangroves in the Philippines, for example, has resulted in a 90%
drop of fisheries production over the 20 years of mangrove removal for shrimp aquaculture, which
was ironically aimed at increasing total fisheries production (Primavera 1997). The devastating
effects of the 2004 Indian Ocean tsunami on many tropical coastal communities underscored the
economic value of mangroves in protection from waves (Koch et al. 2009).

Modeling Biocomplexity and Emergent Properties

Biocomplexity is a synonym for intricacy, but there are differences between complex and com-
plicated systems. For complicated systems, analyses of all subunits are required. For complex
systems, interactions among environmental drivers, transient and nonequilibrium dynamics, as
well as biotic and abiotic interactions and feedback loops must be addressed. Because of the con-
stitutive hierarchy of ecological systems (Hölker & Breckling 2005), it is difficult to separate the
consequences of single factors, processes, and data taken at multiple scales. In such hierarchies,
interactions are nested, which complicates application of the concept of emergence in empirical
studies. IBMs, which are mechanistic models at the level of individuals, have proven suitable for
explaining complex patterns at population levels and for predicting responses to environmental
changes and habitat alterations, which are obscure in population models. In simulation experi-
ments using the gap model FORMAN, trajectories of mangrove attributes were forecast according
to different restoration criteria at Cienega Grande (Colombia) at decadal timescales (Twilley et al.
1998). This study verified mechanisms controlling the rehabilitation of mangroves and contributed
to the design and implementation of restoration projects. Simulation experiments with the IBM
KiWi model (Berger & Hildenbrandt 2000) were used to understand secondary succession of
mangroves in abandoned rice fields in northern Brazil (Berger et al. 2006). This study revealed
that canopy structure was not explained by shade tolerance as originally hypothesized. To match

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 ANRV399-MA02-15 ARI 9 November 2009 16:7

the observed data, growth of the initial dominant species (L. racemosa) had to slow down relative to
the subsequent dominant species (A. germinans). Differences in species-specific NUE (Lovelock
& Feller 2003) may underlie this pattern.
Despite the increasing number of applications of IBMs for understanding mangrove forests
and their responses to disturbances, limitations persist in empirical knowledge and model re-
sources that restrict the use of these as management tools. None of the mangrove forest models
available explicitly include recruitment processes (Berger et al. 2008), which can be important
for regulating forest trajectories over time (Berger et al. 2006). Recruitment limitations linked to
resource availability must be studied to understand how species richness and spatial distribution
are maintained. Small gaps might, for example, restrict regrowth of pioneer species (Baldwin et al.
2001). Simulation studies addressing such issues must be linked across scales to field experiments
focusing on the relationship between gap geometry and species distributions. Multifactorial ex-
periments are needed to examine how hydroperiod and soil nutrient concentration limit growth
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of both seedlings and adult trees (Cardona-Olarte et al. 2006). There is also a need for mechanistic
submodels and hybrid models to support the analyses of field experiments and to serve as input
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modules for environmental conditions in IBMs. Currently, only one model (NUMAN) simulates
soil nutrients for mangrove systems (Chen & Twilley 1998). To address these problems, we need
to combine and test advanced statistical models and mechanistic models, including linkage to
large-scale data sets that allow validation with empirical data.
Most existing IBMs for mangrove forests consider only trees. Similarly for the fauna, only
one IBM describes local movement of crabs (Piou et al. 2007). Developing models that include
food webs and nutrient cycling is a challenge for ecologists and modelers (Cannicci et al. 2008).
Comprehensive analyses of a complex system like mangroves require IBMs that cross trophic
levels and hierarchies.
The description of trees in such models also needs to be improved and to include plant-plant
interactions (Berger & Hildenbrandt 2000), which will provide insights into vegetation dynamics.
Although empirical studies have shown that the relative importance of competition and facilitation
may vary (McKee et al. 2007b), this is not considered in mangrove IBMs.
There is also limitation in the flexibility of plant models (Berger et al. 2008) to represent
plasticity in tree architecture. They are not suitable for analysis of the influence of resprouting or
deviations from circular crown shapes on forest dynamics. Although all mangrove forest models
consider trees, scrub mangroves, such as the low-stature trees frequently occurring on the coastline
or in the hinterlands, are not represented. A model capturing these features would be useful for
analyzing forest dynamics. Inclusion of these will increase technical and scientific requirements
of both empirical and theoretical studies and will also require a multidisciplinary approach.

SUMMARY
Although the concept of emergent properties has been around for a long time, it continues to
provide a framework for identifying and studying key features of an ecosystem that determine its
uniqueness and importance both to science and society. Progress toward identifying key features
and the underlying component processes that are important for improving our understanding
of mangrove responses to climate change, land-use changes, and societal needs requires a more
holistic approach than has been pursued in the past. We need an integrated research strategy
for the future, where empirical and theoretical ecologists as well as computer scientists work
together on formulating, implementing, parameterizing, testing, comparing, and selecting the
new approaches that identify interconnectedness leading to emergent properties. Multidisciplinary
studies are needed that provide the data at different trophic levels and a range of scales, including

410 Feller et al.

 ANRV399-MA02-15 ARI 9 November 2009 16:7

large-scale geographic comparisons, to identify and understand how processes lead to emergent
properties. The development of international networks or observatories that provide large data
sets needed to study variation in emergent properties is essential for moving forward beyond site-
specific studies. Finally, enhanced effectiveness of conservation, restoration, and rehabilitation of
mangrove ecosystems requires an understanding of what leads to desirable emergent properties
that are the most important targets for conservation and restoration. We need to conduct research
to provide the necessary information to design successful projects that will achieve one or more
of these targets.

DISCLOSURE STATEMENT
The authors are not aware of any potential biases that might be perceived as affecting the objectivity
of this review.
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ACKNOWLEDGMENTS
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We apologize in advance to all the investigators whose research we could not appropriately cite
owing to space limitations. If important references were included in recent reviews, we cited the
reviews. We thank Rainer Feller, Anne Chamberlain, and the editorial reviewers of the Annual
Review of Marine Science for helpful edits and comments. This research was funded by the National
Science Foundation (DEB-9981535), the Smithsonian Institution’s Marine Science Network, and
Australian Research Council awards DP0774491 and LP0776680.

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Annual Review of
Marine Science
Contents
Volume 2, 2010

Paleophysical Oceanography with an Emphasis on Transport Rates

Peter Huybers and Carl Wunsch p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
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Advances in Estuarine Physics

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The Effect of Submarine Groundwater Discharge on the Ocean

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Marine Ecomechanics
Mark W. Denny and Brian Gaylord p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p89
Sea Surface Temperature Variability: Patterns and Mechanisms
Clara Deser, Michael A. Alexander, Shang-Ping Xie, and Adam S. Phillips p p p p p p p p p p p p 115
Contemporary Sea Level Rise
Anny Cazenave and William Llovel p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 145
Estimation of Anthropogenic CO2 Inventories in the Ocean
Christopher L. Sabine and Toste Tanhua p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 175
Ocean Deoxygenation in a Warming World
Ralph F. Keeling, Arne Körtzinger, and Nicolas Gruber p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 199
Archaeology Meets Marine Ecology: The Antiquity of Maritime
Cultures and Human Impacts on Marine Fisheries and Ecosystems
Jon M. Erlandson and Torben C. Rick p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 231
The Ecology of Seamounts: Structure, Function, and Human Impacts
Malcolm R. Clark, Ashley A. Rowden, Thomas Schlacher, Alan Williams,
Mireille Consalvey, Karen I. Stocks, Alex D. Rogers, Timothy D. O’Hara,
Martin White,Timothy M. Shank, and Jason M. Hall-Spencer p p p p p p p p p p p p p p p p p p p p p p p 253
Microbial Provinces in the Subseafloor
Matthew O. Schrenk, Julie A. Huber, and Katrina J. Edwards p p p p p p p p p p p p p p p p p p p p p p p p p p 279
Prochlorococcus: Advantages and Limits of Minimalism
Frédéric Partensky and Laurence Garczarek p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 305
Oceanographic and Biogeochemical Insights from Diatom Genomes
Chris Bowler, Assaf Vardi, and Andrew E. Allen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 333

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Genetic Perspectives on Marine Biological Invasions

Jonathan B. Geller, John A. Darling, and James T. Carlton p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 367
Biocomplexity in Mangrove Ecosystems
I.C. Feller, C.E. Lovelock, U. Berger, K.L. McKee, S.B. Joye, and M.C. Ball p p p p p p p p p p p 395
What Can Ecology Contribute to Ecosystem-Based Management?
Simon F. Thrush and Paul K. Dayton p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 419
Bioluminescence in the Sea
Steven H.D. Haddock, Mark A. Moline, and James F. Case p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 443
Annu. Rev. Marine. Sci. 2010.2:395-417. Downloaded from www.annualreviews.org

Errata
by North Carolina State University on 01/21/14. For personal use only.

An online log of corrections to Annual Review of Marine Science articles may be found at
http://marine.annualreviews.org/errata.shtml

Contents vii