3.3 Trophic interactions

3.3.1 Smith, 1987

“Seed predation in relation to tree dominance and distribution in mangrove forests” (Smith 1987)

Key contribution: This is one of the earliest examinations of the effects of predation (by grapsid crabs) on propagule survival for different species. They found significant relationships between propagule predation and nutritional content, as well as location within the intertidal floor. The results led them to conclude that propagule predation is a significant factor in defining zonation in mangrove forests.

Experimental design: Propagules were tethered to twine strings and monitored over 18 days in 5 replicate plots in each of three forest types (high, intermediate and low conspecific dominance) for each of the five species. Additionally, propagules of each of the five species were analyzed for nutritional content and related to predation patterns using PCA.

Key results: The findings show that differential predation for certain species does occur. In particular, predation on A. marina in the mid intertidal was found to explain the relative absence of parent A. marina trees in the mid-intertidal section of the forest. Rates of predation of A. marina were found to be higher than in the low or high intertidal regions.

With the exception of Ceriops tagal, amount of predation was significantly negatively correlated with conspecific dominance (i.e., low dominance by parent trees led to high predation rates) across the other four species.

3.3.2 Smith et al, 1989

“Comparisons of seed predation in tropical, tidal forests from three continents” (Smith et al. 1989)

Key contribution: This study extends (Smith 1987) to examine patterns of propagule predation in four distinct localities: Florida, Panama, Australia and Malaysia. Smith et al conclude that propagule predation has a significant influence on spatial patterning of mangrove species, though to varying degrees depending on propagule species and also species of predator.

Smith et al term the hypothesis that spatial assemblages are a result of predation as the “dominance-predation” model.

Study design: Following the methods of (Smith 1987), replicate plots with secured propagules were established in stands with dominance of propagule parent trees and absence of propagule parent trees. The seedlings were monitored for 4 days to identify predation such that they are incapable of establishing (i.e., 50% mass consumed, taken down hole, or radicle and hypocotyl consumed).

Key results: The study confirms the prior work in that species of Avicennia were completely consumed in stands in which their parent trees were rare or absent, but not consumed in stands where they were abundant.

The findings for Rhizophora species were a bit more mixed, with the “dominance-predation” model holding true in Malaysia and Australia, but failing in the North American sites. In Florida, no Rhizophora propagules were consumed. In Panama, more propagules were consumed in the Rhizophora-dominated site relative to the Avicennia-dominated site.

More Bruguiera propagules were consumed where it was rare than it was common in Malaysia, and the reverse held true for Australia.

Differences in predator distribution may explain some of the variability. In particular, grapsid crabs did not exist at the site in Florida, which may explain lack of consumption of Rhizophora. In forests with only snail consumers, only Avicennia were consumed.

This may be a result of the feeding mechanisms of crabs versus snail, and the physical structure of Rhizophora vs. Avicennia propagules (i.e., crabs are able to rip through tough hypocotyl of Rhizophora propagules).

3.3.3 Cannicci et al, 2008

“Faunal impact on vegetation structure and ecosystem function in mangrove forests: A review” (Cannicci et al. 2008)

Key contribution: This is a well-written review on faunal impacts on forest structure and ecosystem function within mangroves. It does not necessarily relate to purely herbivory (which many of the studies related to mangrove predation do), but also considers some of the community ecology aspects important for ecosytem functioning.

Key notes:

Insects - Most common forms of insect herbivory are:

1. Leaf-feeding - can be very significant and produce massive leaf-loss events
2. Wood-boring - very limited evidence (Feller in Belize), but has found to produce leaf-loss as great or greater than direct leaf herbivory. Insects bore wood on branches and leaves along the branch are subsequently lost, which can create significant canopy gaps
3. Flower/fruit/seed-feeding - may be a result of reduced biomass allocation to reproductive tissues following leaf herbivory or other damage; or may be a result of direct feeding on propagules

The costs of leaf herbivory and stress on the plant are a function of both the direct impacts, as well as the additional biomass and resources needed to be put into regenerating leaves or building defensive mechanisms. Toxins (E. allagocha; Euphorbiaceae), tannins or thicker leaves may require resource inputs that could otherwise be allocated towards growth.

Ants are the most dominant insects in mangroves, both numerically and energetically, despite the difficult floor conditions in which many require. Ant communities consist of both terrestrial species as well as those endemic to mangroves.

Although data is limited, studies have shown that ants in mangroves can significantly reduce the presence of herbivorous pests (note that this is decoupled from improving plant “performance” per se).

Crabs - Feeding patterns of crabs vary by species within mangrove. Some predominantly feed on leaf litter, whereas others have adopted arborial life styles and feed largely on green leaves. They scrape the leaves which likely has similar impacts on tree fitness as other herbivores.

Crabs understood as main agents of high leaf litter turnover in mangroves. In particular, sesarmid crabs in Southeast Asia are main consumers of leaf litter, though magnitude of influence is highly variable.

In Neotropics, ocypodidae crabs are found to be most influential on leaf litter dynamics.

In general, however, feeding behavior of crabs is poorly understood within mangroves.

Biomass cycling of crabs:

1. Low assimilation rates of leaf litter (<50%)
2. Additionally, approximately 60% of dry weight is defecated
   • Crab fecal matter may be of higher nutritional content than leaf litter, acting as food source for benthic organisms
   • Shredding of leaves occurs, and bacterial diversity on crab fecal matter found to be 70 times greater than that of raw leaf litter

“Reduced competition from crabs” - Several mechanisms have been proposed for reductions in seedling/sapling competition due to propagule predation:

1. Predation-dependence model - inverse relationship between rate of predation and dominance of particular species
   • Smith has found support for it, whereas a number of other studies have found a lack of evidence in support of the hypothesis and thus have proposed alternative mechanisms
2. Canopy-gap mediated model - hypothesizes that predation is more intense under closed canopies than in light gaps
   • Has led some to propose a “mutualism” between sesarmid crabs and mangrove trees in that crabs reduce competition and allow established saplings to compete while mangroves provide food
3. Flooding regime model - time for terrestrial foragers is limited due to variation in exposure of the forest floor
   • Sousa found otherwise

“Bioturbation of soil” - Impacts of crabs as ecosystem engineers may have strong implications for soil quality within mangroves:

• Sesarmid crabs were found to significantly reduce aluminum and sulfur contents of soil
• Fiddler crabs may increase the depth of iron reduction
• Burrowing create preferential flow pathways which may flush out accumulated salts, particularly within rhizospheres

Molluscs - Most well represented taxon along with decapod crustaceans, however their ecological role is poorly understood.

• Snails can be significant feeders of leaf-litter, feeding during both low and high tides in which they chemically sense leaves underwater
• Sponges may play a role in inducing growth of adventitious rootlets that absorb ammonium and other nitrogenous compounds
• Oysters and barnacles may have negative effects on root growth, and may also result in breaking of roots due to harvesting by humans

3.3.4 Sousa, 2011

“Trophic interactions in coastal and estuarine mangrove forest ecosystems” (Sousa and Dangremond 2011)

Key contribution: This is an extensive review on trophic interactions in mangroves. It extends beyond conventional consideration of herbivory and the effects of trophic interactions on forest structure by including discussion of faunal interactions.

Productivity - Mangroves have been found to have higher aboveground net primary productivity rates (mean ~14 Mg DW / ha) than terrestrial tropical forests (mean 5 Mg DW / ha).

Methods of measuring NPP are varied and inaccurate, and thus the estimates provided within the literature are likely to be quite coarse. Little research has examined the productivity of phytoplankton in tidal waters or cyanobacteria on aboveground root systems, though some studies have shown this to be half or more of ecosystem productivity.

Herbivory - Primary component of energy flow through ecosystem, yet relatively unstudied within mangrove ecosystems.

Insect herbivory - General consensus is that insect herbivory is not a significant consideration, although this is likely based on little evidence. Methodological issues constrain our current estimates of the degree of leaf herbivory by insects.

Of the studies that exist, rates of leaf removal are relatively low at 7.6% for Avicennia spps and 5% for Rhizophora spps. Longitudinal studies that have followed leaf herbivory through the duration of its development (from bud to the end of the study period) have found herbivory rates to be much higher (10-30%).

Additionally, occasional mass herbivory events due to emergence of lepidopterans can defoliate massive expanses of trees. Caterpillars emerge and within three months trees have lost > 75% of foliage.

Crab herbivory - Majority of crabs forage on forest floor, but some exhibit (almost) purely arborial habits Some are found in both terrestrial and low tree canopies, whereas four species of sesarmid crabs are purely arboreal (come to floor rarely if ever).

1. Aratus pisonii - Atlantic/Caribbean/Eastern Pacific; feeds on young leaves largely from R mangle
2. Parasesarma leptosoma - Indo-West Pacific; feeds on young leaves
3. Armases elegans - West Africa, feeds on young leaves
4. Selatium brockii - Feeds on algae growing on tree trunks

Stem boring - wood-eating beetles and moths can have significant impacts on forest structure, particularly through the opening of small gaps within the forest via death of branches.

Coccotrypes rhizophorae - Rhizophora specialist beetle that bores roots, wood and propagules; can change morphology of root systems (Atlantic/Caribbean/Eastern Pacific)

Coccotrypes fallax - the congener to C rhizophorae in the Indo-West Pacific

Propagule predation - Propagule predation may occur before or after dispersal:

• “Predispersal predation” occurs when propagules are still on parent trees. Often have boring insects (e.g., C. rhizophorae) which may ultimately cause premature dropping of propagules, their death, or reduced growth rates of seedlings following establishment. C. rhizophorae lay eggs in Rhizophora propagules and can greatly damage the propagules.
• “Postdispersal predation” - a relative boom in research following Smith’s tethered propagules studies. Although findings corroborate with his conclusions per Avicennia propagules in some cases, other studies have shown the predation-dependence model to not hold true.

Detrivory and decomposition:

Outwelling hypothesis - idea that substantial amounts of organic matter are exported to adjacent estuaries, which supports dense populations of detritivores and secondary and tertiary consumers

Odum and Heald’s work in Florida exemplified the process by which outwelling of organic matter in mangroves may occur:

1. Mangrove leaf litter drops and undergoes decomposition by bacteria, fungi and protozoa
2. Crabs and other detritivores further consume leaf litter, breaking it up into finer pieces
3. Organic matter in fine, processed form is exported via tidal flows
4. Exported OM fuels marine and detritus-based food chains (postulated)

The importance of this particular pathway has since been questioned, as supporting evidence has been largely been circumstantial. The circumstantial evidence of this pathway may indicate a large contribution of DOC.

Outwelling of OM likely occurs in most tidally inundated and riverine forests, though the degree to which it happens depends on site, season and years.

Different patterns of outwelling exist for basin forests separated by berms, in which only highest tides flush the system, versus riverine or fringe forests that undergo more periodic flushing.

Retention and recycling of carbon and nitrogen - export of organic matter and nutrients is also greatly controlled by recycling of nutrients within the system.

Detritus-feeding crustaceans - A review of studies finds that, on average, 57% of detritus is either consumed or buried by crabs.

Studies have found a strong preference by crabs for older, more decomposed leaf litter in which C:N ratios are much lower, and tannin content and toughness of the leaf are much reduced. Nevertheless, the C:N ratio is still quite high and thus crabs likely need to look for additional N sources. Studies have suggested that this may come from grazing on algae or predation of animal tissue (crustaceans, mollusks, annelids, insects and fish).

Detritus-feeding mollusks - consumption of detritus by mollusks can be significant in addition to that of crustaceans.

Deposit-feeding crabs - largely comprise of fiddler crabs; feed on bacteria, microalgae and detrital material (often bacteria, smaller diatoms and protozoa); assimilation efficiency is much higher for bacteria than microalgae

Litter decomposition - the nutritional content of leaves from different species varies, but in general decomposition improves the nutritional quality over time. Tannins are high but are leached from the leaf quite rapidly; following leaching of soluble compounds, lignocellulose is primary component; bacteria digest lignocellulose at a much faster rate than other decomposters, and animals cannot digest lignocellulose

Wood and root decomposition - a higher proportion of lignocellulose exists in wood and roots, thus decomposition is much slower than for leaves.

Little is known about the functional groups and diversity of fungi in mangroves, but they may play a significant role in decomposition of wood and roots. Additionally, wood-boring insects with mutualistic relationships with bacteria that can process lignocellulose may be important for decomposition of woody biomass (e.g., termites).

Predation - In addition, the review provides a discussion of predator-prey interactions but I have not included notes here as it is beyond the direct scope of the qualifying exam.

References

Smith, Thomas J. 1987. “Seed Predation in Relation to Tree Dominance and Distribution in Mangrove Forests.” Ecology 68 (2): 266–73. doi:10.2307/1939257.

Smith, Thomas J, Hung T Chan, Carole C McIvor, and Michael B Robblee. 1989. “Comparisons of Seed Predation in Tropical, Tidal Forests from Three Continents.” Ecology 70 (1): 146–51. doi:10.2307/1938421.

Cannicci, Stefano, Damien Burrows, Sara Fratini, Thomas J Smith, Joachim Offenberg, and Farid Dahdouh-Guebas. 2008. “Faunal Impact on Vegetation Structure and Ecosystem Function in Mangrove Forests: A Review.” Aquatic Botany 89 (2): 186–200. doi:10.1016/j.aquabot.2008.01.009.

Sousa, Wayne, and Emily Dangremond. 2011. “Trophic Interactions in Coastal and Estuarine Mangrove Forest Ecosystems.” In Treatise on Estuarine and Coastal Science, Volume 6, 43–93. Elsevier Inc. doi:10.1016/B978-0-12-374711-2.00606-9.