skip to main content


Title: Introduced mangroves escape damage from marine and terrestrial enemies
Abstract

The enemy release hypothesis (ERH) posits that introduced species often leave their enemies behind when introduced to a new range. This release from enemies may allow introduced species to achieve higher growth and reproduction and may explain why some invaders flourish in new locations. Red mangroves (Rhizophora mangle) were introduced to Hawaiʻi from Florida over a century ago. Because Hawaiʻi has no native mangroves, the arrival ofR. manglefundamentally changed the structure and function of estuarine shorelines. While numerous enemies affect red mangroves in their native range (tropical America), in Hawaiʻi, mangroves apparently experience little herbivory, which may explain why introduced mangroves are so productive, fecund, and continue to spread. In this study, we compared the effects of enemies in native and introduced populations of brackish red mangroves (R. mangle) in 8–10 sites in the native range (Florida, Belize, and Panama) and introduced range of mangroves (Hawaiʻi). At each site, we measured the (1) occurrence of enemies using timed visual surveys, (2) occurrence of damage to different mangrove structures (leaves, apical buds, dead twigs, roots, propagules, and seedlings), and (3) rate of propagule herbivory using tethering experiments. Consistent with the ERH, we found an order of magnitude less damage and fewer enemies in introduced than native mangrove sites. While introduced mangroves harbored few enemies and minimal damage, native mangroves were affected by numerous enemies, including leaf‐eating crabs, specialist bud moths, wood‐boring insects and isopods, and propagule predators. These patterns were consistent across all plant structures (roots to leaves), among marine and terrestrial enemies, and across functional groups (browsers, borers, pathogens, etc.), which demonstrates enemy escape occurs consistently among different functional groups and via trophic (e.g., herbivores) and non‐trophic (e.g., root borers) interactions. Our study is among the first biogeographical enemy release studies to take a comprehensive approach to quantifying the occurrence of damage from a broad suite of marine and terrestrial taxa across an array of wetland plant structures. Understanding how natural enemies alter this key foundation species will become increasingly relevant globally as mangroves continue to invade new regions through intentional plantings or range expansion driven by climate change.

 
more » « less
NSF-PAR ID:
10365280
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology
Volume:
103
Issue:
3
ISSN:
0012-9658
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Top‐down effects of predators and bottom‐up effects of resources are important drivers of community structure and function in a wide array of ecosystems. Fertilization experiments impose variation in resource availability that can mediate the strength of predator impacts, but the prevalence of such interactions across natural productivity gradients is less clear. We studied the joint impacts of top‐down and bottom‐up factors in a tropical mangrove forest system, leveraging fine‐grained patchiness in resource availability and primary productivity on coastal cays of Belize. We excluded birds from canopies of red mangrove (Rhizophoraceae:Rhizophora mangle) for 13 months in zones of phosphorus‐limited, stunted dwarf mangroves, and in adjacent zones of vigorous mangroves that receive detrital subsidies. Birds decreased total arthropod densities by 62%, herbivore densities more than fivefold, and reduced rates of leaf and bud herbivory by 45% and 52%, respectively. Despite similar arthropod densities across both zones of productivity, leaf and bud damage were 2.0 and 4.3 times greater in productive stands. Detrital subsidies strongly impacted a suite of plant traits in productive stands, potentially making leaves more nutritious and vulnerable to damage. Despite consistently strong impacts on herbivory, we did not detect top‐down forcing that impacted mangrove growth, which was similar with and without birds. Our results indicated that both top‐down and bottom‐up forces drive arthropod community dynamics, but attenuation at the plant‐herbivore interface weakens top‐down control by avian insectivores.

     
    more » « less
  2. Abstract

    The rapid human‐driven changes in the environment during the Anthropocene have placed extreme stress on many plants and animals. Beneficial interactions with microorganisms may be crucial for ameliorating these stressors and facilitating the ecosystem services host organisms provide. Foliar endophytes, microorganisms that reside within leaves, are found in essentially all plants and can provide important benefits (e.g., enhanced drought tolerance or resistance to herbivory). However, it remains unclear how important the legacy effects of the abiotic stressors that select on these microbiomes are for affecting the degree of stress amelioration provided to their hosts. To elucidate foliar endophytes' role in host‐plant salt tolerance, especially if salinity experienced in the field selects for endophytes that are better suited to improve the salt tolerance of their hosts, we combined field collections of 90 endophyte communities from 30 sites across the coastal Everglades with a manipulative growth experiment assessing endophyte inoculation effects on host‐plant performance. Specifically, we grew >350 red mangrove (Rhizophora mangle) seedlings in a factorial design that manipulated the salinity environment the seedlings experienced (freshwater vs. saltwater), the introduction of field‐collected endophytes (live vs. sterilized inoculum), and the legacy of salinity stress experienced by these introduced endophytes, ranging from no salt stress (0 parts per thousand [ppt] salinity) to high salt stress (40 ppt) environments. We found that inoculation with field‐collected endophytes significantly increased mangrove performance across almost all metrics examined (15%–20% increase on average), and these beneficial effects typically occurred when the endophytes were grown in saltwater. Importantly, our study revealed the novel result that endophyte‐conferred salinity tolerance depended on microbiome salinity legacy in a key coastal foundation species. Salt‐stressed mangroves inoculated with endophyte microbiomes from high‐salinity environments performed, on average, as well as plants grown in low‐stress freshwater, while endophytes from freshwater environments did not relieve host salinity stress. Given the increasing salinity stress imposed by sea level rise and the importance of foundation species like mangroves for ecosystem services, our results indicate that consideration of endophytic associations and their salinity legacy may be critical for the successful restoration and management of coastal habitats.

     
    more » « less
  3. Ecological regime shifts are expected to increase this century as climate change propagates cascading effects across ecosystems with coupled elements. Here, we demonstrate that the climate-driven salt marsh–to–mangrove transition does not occur in isolation but is linked to lesser-known oyster reef–to–mangrove regime shifts through the provision of mangrove propagules. Using aerial imagery spanning 82 y, we found that 83% of oyster reefs without any initial mangrove cover fully converted to mangrove islands and that mean (± SD) time to conversion was 29.1 ± 9.6 y. In situ assessments of mangrove islands suggest substantial changes in ecosystem structure during conversion, while radiocarbon dates of underlying reef formation indicate that such transitions are abrupt relative to centuries-old reefs. Rapid transition occurred following release from freezes below the red mangrove ( Rhizophora mangle ) physiological tolerance limit (−7.3 °C) and after adjacent marsh-to-mangrove conversion. Additional nonclimate-mediated drivers of ecosystem change were also identified, including oyster reef exposure to wind-driven waves. Coupling of regime shifts arises from the growing supply of mangrove propagules from preceding and adjacent marsh-to-mangrove conversion. Climate projections near the mangrove range limit on the Gulf coast of Florida suggest that regime shifts will begin to transform subtropical estuaries by 2070 if propagule supply keeps pace with predicted warming. Although it will become increasingly difficult to maintain extant oyster habitat with tropicalization, restoring oyster reefs in high-exposure settings or active removal of mangrove seedlings could slow the coupled impacts of climate change shown here. 
    more » « less
  4. Mangrove forests along the coastlines of the tropical and sub-tropical western Atlantic are intermittently impacted by hurricanes and can be damaged by high-speed winds, high-energy storm surges, and storm surge sediment deposits that suffocate tree roots. This study quantified trends in damage, delayed mortality, and early signs of below- and aboveground recovery in mangrove forests in the Lower Florida Keys and Ten Thousand Islands following direct hits by Hurricane Irma in September 2017. Mangrove trees suffered 19% mortality at sites in the Lower Florida Keys and 11% in the Ten Thousand Islands 2–3 months post-storm; 9 months post-storm, mortality in these locations increased to 36% and 20%, respectively. Delayed mortality of mangrove trees was associated with the presence of a carbonate mud storm surge deposit on the forest floor. Mortality and severe branch damage were more common for mangrove trees than for mangrove saplings. Canopy coverage increased from 40% cover 1–2 months post-storm to 60% cover 3–6 months post-storm. Canopy coverage remained the same 9 months post-storm, providing light to an understory of predominantly Rhizophora mangle (red mangrove) seedlings. Soil shear strength was higher in the Lower Florida Keys and varied with depth; no significant trends were found in shear strength between fringe or basin plots. Rates of root growth, as assessed using root in-growth bags, were relatively low at 0.01–11.0 g m−2 month−1 and were higher in the Ten Thousand Islands. This study demonstrated that significant delayed mangrove mortality can occur 3–9 months after a hurricane has passed, with some mortality attributable to smothering by storm surge deposits. 
    more » « less
  5. Abstract

    Resident species can facilitate invading species (biotic assistance) or inhibit their expansion (biotic resistance). Species interactions are often context‐dependent and the relative importance of biotic assistance versus resistance could vary with abiotic conditions or the life stage of the invading species, as invader stress tolerances and resource requirements change with ontogeny. In northeast Florida salt marshes, the abundant dead litter (wrack) of the native marsh cordgrass,Spartina alterniflora, could influence the expansion success of the black mangrove,Avicennia germinans, a tropical species that is expanding its range northward.

    We used two field experiments to examine howS. alterniflorawrack affectsA. germinanssuccess during (a) propagule establishment and (b) subsequent seedling survival. We also conducted laboratory feeding assays to identify propagule consumers and assess how wrack presence influences herbivory on mangrove propagules.

    Spartina alterniflorawrack facilitatedA. germinansestablishment by promoting propagule recruitment, retention and rooting; the tidal regime influenced the magnitude of these effects. However, over timeS. alterniflorawrack inhibitedA. germinansseedling success by smothering seedlings and attracting herbivore consumers. Feeding assays identified rodents—which seek refuge in wrack—as consumers ofA. germinanspropagules.

    Synthesis. Our results suggest that the deleterious effects ofS. alterniflorawrack onA. germinansseedling survival counterbalance the initial beneficial effects of wrack onA. germinansseed establishment. Such seed‐seedling conflicts can arise when species stress tolerances and resource requirements change throughout development and vary with abiotic conditions. In concert with the tidal conditions, the relative importance of positive and negative interactions with wrack at each life stage can influence the rate of local and regional mangrove expansion. Because interaction strengths can change in direction and magnitude with ontogeny, it is essential to examine resident–invader interactions at multiple life stages and across environmental gradients to uncover the mechanisms of biotic assistance and resistance during invasion.

     
    more » « less