pathogens of multiple marine fishes and invertebrates in seawater was lower when seagrass was present compared with the paired site
without seagrass (generalized linear model, estimate ± SEstatus × location = –0.790 ± 0.221, P < 0.001)
(Fig. 2A and table S7). The relative abundance of
bacterial pathogens in seawater from the intertidal flat was 50% lower within the seagrass meadow compared to the paired site (generalized
linear model, Z = 2.061, P = 0.039) and 50% lower
in seawater from the coral reef adjacent to the
seagrass meadow compared with the paired site
(generalized linear model, Z = 4.098, P < 0.001)
(Fig. 2, A to C, and table S8). Assemblages of potential bacterial pathogens (assessed by composition and relative abundance) formed two clear
groups (representing 94.8% of the total assemblage variability with 79% similarity among group
replicates) and differed significantly between the
paired seagrass present and absent sites [per-mutational multivariate analysis of variance (
per-MANOVA), Fig. 2D]. The separations between the
groups (determined by Pearson correlations ≥
0.6) were associated with higher relative abundance of Flavobacterium, Corynebacterium, Vibrio,
Rickettsia, and Shewanella at sites where seagrass
meadows were absent (Fig. 2, B to D; fig. S4; and
Effective treatment of municipal sewage and a
broad range of industrial wastewater treatments
using natural ecosystem services have been linked
to reductions in preventable waterborne human
diseases (13). However, there have been no studies
to evaluate this effect for diseases that affect
marine organisms. Seagrass meadows and coral
reefs are tightly linked habitats (14) and provide
an opportunity to assess this effect in situ. We
visually examined 8034 reef-building corals for
visual signs of tissue loss characteristic of active
disease lesions (15) along reefs with adjacent seagrass meadows and paired reefs without adjacent
seagrass meadows at all four islands (fig. S1 and
table S1, benthic area surveyed = 360 m2). Overall
coral disease prevalence was 50% less on reefs
with adjacent seagrass meadows (mean ± SE =
1.6 ± 0.6%, range = 0 to 2%) than on paired reefs
without adjacent seagrass meadows (3.9 ± 1.2%,
range = 1 to 7%; generalized linear mixed model,
Z = –4.213, P < 0.001, n = 4 islands) (Fig. 3). Two
of five globally occurring coral diseases, white
syndrome and black band disease, as well as
signs of coral tissue mortality associated with
bleaching and sediment deposition, were significantly less on reefs adjacent to seagrass meadows
compared with paired reefs (generalized linear
mixed model, Fig. 3 and table S10).
Our results indicated that seagrass meadows
significantly reduce bacterial loads and can benefit both humans and other organisms in the environment. Represented on every continental shelf
but Antarctica, seagrasses are valued for (16) nutrient cycling, sediment stabilization, reducing the
effects of carbon dioxide elevation, and providing
nursery habitat for fisheries.
Our observation of reduced levels of coral dis-
ease on reefs adjacent to seagrass meadows offers
independent support of the benefits that seagrass
meadows provide to controlling pathogenic bac-
teria in marine environments. Although determin-
ing the mechanisms involved will require further
research, sediment retention by seagrass mead-
ows (16) could play an integral role in ameliorat-
ing disease. Sediment-associated bacteria have been
identified as a potential source of coral pathogens
from marine and terrestrial substrates (17). Both
black band disease (18) and white syndromes (19)
have been linked to elevated levels of sediment
exposure in situ.
Outbreaks of diseases that affect reef-building
corals have recently emerged as a considerable
driver of global coral reef degradation (20), with
losses in the Caribbean and Indo-Pacific approx-
imating 50 to 80%. For example, one bacterial pa-
thogen isolated from sewage, Serratia marcescens,
is linked to the decline of two dominant reef-
building corals now on the U.S. endangered species
list and subsequent ecological phase shifts from
coral- to algal-dominated reefs (21). Regardless
of the exact mechanisms involved, alleviating coral
disease is vital for the well-being and livelihoods of
275 million people living within 30 km of a coral
reef (22), as well as being of direct benefit to reef-
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This research was supported by The Nature Conservancy
NatureNet Fellowship, Atkinson Center for a Sustainable Future
at Cornell University, and the Capturing Coral Reef and Ecosystem
Related Services (CCRES) Project funded by the Global Environment
Facility and the World Bank (Project ID P123933). We thank R. Yoshioka
and A. Tracy, A. Massinai, R. Ambo-Rappe, A. Ahmad, S. Beveridge, and
S. Steven for statistical, laboratory, and field assistance. Vector
illustrations are credited to T. Saxby of the Integration and Application
Network at the University of Maryland Center for Environmental
Science and Shutterstock contributors R. A. Hillman (image ID
25377103) and K. Ka (image ID 250306321). We acknowledge village
community members for their permission to conduct this study
through Hasanuddin University. Sequence data are archived at the
National Center for Biotechnology Information (accession no.
SRP095480). Data and code are available at the Dryad Digital
Materials and Methods
Figs. S1 to S4
Tables S1 to S10
16 October 2016; accepted 23 January 2017
Hawkmoths use nectar sugar to
reduce oxidative damage from flight
E. Levin,1 G. Lopez-Martinez,2 B. Fane,3 G. Davidowitz1
Nectar-feeding animals have among the highest recorded metabolic rates. High aerobic
performance is linked to oxidative damage in muscles. Antioxidants in nectar are scarce to
nonexistent. We propose that nectarivores use nectar sugar to mitigate the oxidative damage
caused by the muscular demands of flight. We found that sugar-fed moths had lower oxidative
damage to their flight muscle membranes than unfed moths. Using respirometry coupled with
d13C analyses, we showed that moths generate antioxidant potential by shunting nectar glucose
to the pentose phosphate pathway (PPP), resulting in a reduction in oxidative damage to the
flight muscles. We suggest that nectar feeding, the use of PPP, and intense exercise are causally
linked and have allowed the evolution of powerful fliers that feed on nectar.
Floral nectar is the primary nutrient source for many taxa, including birds, insects, and mammals. Nectar is energy rich, consisting predominantly of water and carbohydrates (1) with little to no antioxidant components
(2). Foraging for nectar often involves metabol-
ically expensive flight or hovering. Hovering flight
is the most energetically expensive form of loco-
motion known (3), with metabolic rates reach-
ing 170 times higher than at rest (4). To fuel their
flight muscles, nectarivores oxidize energy-rich
molecules, often a combination of fuel types.