Plasticity is a locally adapted trait with consequences for ecological dynamics in novel environments

Phenotypic plasticity is predicted to evolve in more variable environments, conferring an advantage on individual lifetime fitness. It is less clear what the potential consequences of that plasticity will have on ecological population dynamics. Here, we use an invertebrate model system to examine the effects of environmental variation (resource availability) on the evolution of phenotypic plasticity in two life history traits—age and size at maturation—in long‐running, experimental density‐dependent environments. Specifically, we then explore the feedback from evolution of life history plasticity to subsequent ecological dynamics in novel conditions. Plasticity in both traits initially declined in all microcosm environments, but then evolved increased plasticity for age‐at‐maturation, significantly so in more environmentally variable environments. We also demonstrate how plasticity affects ecological dynamics by creating founder populations of different plastic phenotypes into new microcosms that had either familiar or novel environments. Populations originating from periodically variable environments that had evolved greatest plasticity had lowest variability in population size when introduced to novel environments than those from constant or random environments. This suggests that while plasticity may be costly it can confer benefits by reducing the likelihood that offspring will experience low survival through competitive bottlenecks in variable environments. In this study, we demonstrate how plasticity evolves in response to environmental variation and can alter population dynamics—demonstrating an eco‐evolutionary feedback loop in a complex animal moderated by plasticity in growth.     

Effects of Nano-Titanium Dioxide on Freshwater Algal Population Dynamics

To make predictions about the possible effects of nanomaterials across environments and taxa, toxicity testing must incorporate not only a variety of organisms and endpoints, but also an understanding of the mechanisms that underlie nanoparticle toxicity. Here, we report the results of a laboratory experiment in which we examined how titanium dioxide nanoparticles impact the population dynamics and production of biomass across a range of freshwater algae. We exposed 10 of the most common species of North American freshwater pelagic algae (phytoplankton) to five increasing concentrations of n-TiO₂ (ranging from controls to 300 mg n-TiO₂ L⁻¹). We then examined the effects of n-TiO₂ on the population growth rates and biomass production of each algal species over a period of 25 days. On average, increasing concentrations of n-TiO₂ had no significant effects on algal growth rates (p = 0.376), even though there was considerable species-specific variation in responses. In contrast, exposure to n-TiO₂ tended to increase maximum biomass achieved by species in culture (p = 0.06). Results suggest that titanium dioxide nanoparticles could influence certain aspects of population growth of freshwater phytoplankton, though effects are unlikely at environmentally relevant concentrations.     

Host ecotype generates evolutionary and epidemiological divergence across a pathogen metapopulation

The extent and speed at which pathogens adapt to host resistance varies considerably. This presents a challenge for predicting when—and where—pathogen evolution may occur. While gene flow and spatially heterogeneous environments are recognized to be critical for the evolutionary potential of pathogen populations, we lack an understanding of how the two jointly shape coevolutionary trajectories between hosts and pathogens. The rust pathogen Melampsora lini infects two ecotypes of its host plant Linum marginale that occur in close proximity yet in distinct populations and habitats. In this study, we found that within-population epidemics were different between the two habitats. We then tested for pathogen local adaptation at host population and ecotype level in a reciprocal inoculation study. Even after controlling for the effect of spatial structure on infection outcome, we found strong evidence of pathogen adaptation at the host ecotype level. Moreover, sequence analysis of two pathogen infectivity loci revealed strong genetic differentiation by host ecotype but not by distance. Hence, environmental variation can be a key determinant of pathogen population genetic structure and coevolutionary dynamics and can generate strong asymmetry in infection risks through space.     

Demographic Inference Reveals African and European Admixture in the North American Drosophila melanogaster Population

Drosophila melanogaster spread from sub-Saharan Africa to the rest of the world colonizing new environments. Here, we modeled the joint demography of African (Zimbabwe), European (The Netherlands), and North American (North Carolina) populations using an approximate Bayesian computation (ABC) approach. By testing different models (including scenarios with continuous migration), we found that admixture between Africa and Europe most likely generated the North American population, with an estimated proportion of African ancestry of 15%. We also revisited the demography of the ancestral population (Africa) and found—in contrast to previous work—that a bottleneck fits the history of the population of Zimbabwe better than expansion. Finally, we compared the site-frequency spectrum of the ancestral population to analytical predictions under the estimated bottleneck model.     

Diversity of environmental single-stranded DNA phages revealed by PCR amplification of the partial major capsid protein

The small single-stranded DNA (ssDNA) bacteriophages of the subfamily Gokushovirinae were traditionally perceived as narrowly targeted, niche-specific viruses infecting obligate parasitic bacteria, such as Chlamydia. The advent of metagenomics revealed gokushoviruses to be widespread in global environmental samples. This study expands knowledge of gokushovirus diversity in the environment by developing a degenerate PCR assay to amplify a portion of the major capsid protein (MCP) gene of gokushoviruses. Over 500 amplicons were sequenced from 10 environmental samples (sediments, sewage, seawater and freshwater), revealing the ubiquity and high diversity of this understudied phage group. Residue-level conservation data generated from multiple alignments was combined with a predicted 3D structure, revealing a tendency for structurally internal residues to be more highly conserved than surface-presenting protein–protein or viral–host interaction domains. Aggregating this data set into a phylogenetic framework, many gokushovirus MCP clades contained samples from multiple environments, although distinct clades dominated the different samples. Antarctic sediment samples contained the most diverse gokushovirus communities, whereas freshwater springs from Florida were the least diverse. Whether the observed diversity is being driven by environmental factors or host-binding interactions remains an open question. The high environmental diversity of this previously overlooked ssDNA viral group necessitates further research elucidating their natural hosts and exploring their ecological roles.     

Evidence of Natural Selection Acting on a Polymorphic Hybrid Incompatibility Locus in Mimulus

As a common cause of reproductive isolation in diverse taxa, hybrid incompatibilities are fundamentally important to speciation. A key question is which evolutionary forces drive the initial substitutions within species that lead to hybrid dysfunction. Previously, we discovered a simple genetic incompatibility that causes nearly complete male sterility and partial female sterility in hybrids between the two closely related yellow monkeyflower species Mimulus guttatus and M. nasutus. In this report, we fine map the two major incompatibility loci—hybrid male sterility 1 (hms1) and hybrid male sterility 2 (hms2)—to small nuclear genomic regions (each <70 kb) that include strong candidate genes. With this improved genetic resolution, we also investigate the evolutionary dynamics of hms1 in a natural population of M. guttatus known to be polymorphic at this locus. Using classical genetic crosses and population genomics, we show that a 320-kb region containing the hms1 incompatibility allele has risen to intermediate frequency in this population by strong natural selection. This finding provides direct evidence that natural selection within plant species can lead to hybrid dysfunction between species.     

Hybridization masks speciation in the evolutionary history of the Galápagos marine iguana

The effects of the direct interaction between hybridization and speciation—two major contrasting evolutionary processes—are poorly understood. We present here the evolutionary history of the Galápagos marine iguana (Amblyrhynchus cristatus) and reveal a case of incipient within-island speciation, which is paralleled by between-island hybridization. In-depth genome-wide analyses suggest that Amblyrhynchus diverged from its sister group, the Galápagos land iguanas, around 4.5 million years ago (Ma), but divergence among extant populations is exceedingly young (less than 50 000 years). Despite Amblyrhynchus appearing as a single long-branch species phylogenetically, we find strong population structure between islands, and one case of incipient speciation of sister lineages within the same island—ostensibly initiated by volcanic events. Hybridization between both lineages is exceedingly rare, yet frequent hybridization with migrants from nearby islands is evident. The contemporary snapshot provided by highly variable markers indicates that speciation events may have occurred throughout the evolutionary history of marine iguanas, though these events are not visible in the deeper phylogenetic trees. We hypothesize that the observed interplay of speciation and hybridization might be a mechanism by which local adaptations, generated by incipient speciation, can be absorbed into a common gene pool, thereby enhancing the evolutionary potential of the species as a whole.     

A new North American therizinosaurid and the role of herbivory in ‘predatory’ dinosaur evolution

Historically, ecomorphological inferences regarding theropod (i.e. ‘predatory’) dinosaurs were guided by an assumption that they were singularly hypercarnivorous. A recent plethora of maniraptoran discoveries has produced evidence challenging this notion. Here, we report on a new species of maniraptoran theropod, Nothronychus graffami sp. nov. Relative completeness of this specimen permits a phylogenetic reassessment of Therizinosauria—the theropod clade exhibiting the most substantial anatomical evidence of herbivory. In the most comprehensive phylogenetic study of the clade conducted to date, we recover Therizinosauria as the basalmost maniraptoran lineage. Using concentrated changes tests, we present evidence for correlated character evolution among herbivorous and hypercarnivorous taxa and propose ecomorphological indicators for future interpretations of diet among maniraptoran clades. Maximum parsimony optimizations of character evolution within our study indicate an ancestral origin for dietary plasticity and facultative herbivory (omnivory) within the clade. These findings suggest that hypercarnivory in paravian dinosaurs is a secondarily derived dietary specialization and provide a potential mechanism for the invasion of novel morpho- and ecospace early in coelurosaurian evolution—the loss of obligate carnivory and origin of dietary opportunism.     

Adaptive basis of geographic variation: genetic,phenotypic and environmental differences among beach mouse populations

A major goal in evolutionary biology is to understand how and why populations differentiate, both genetically and phenotypically, as they invade a novel habitat. A classical example of adaptation is the pale colour of beach mice, relative to their dark mainland ancestors, which colonized the isolated sandy dunes and barrier islands on Florida''s Gulf Coast. However, much less is known about differentiation among the Gulf Coast beach mice, which comprise five subspecies linearly arrayed on Florida''s shoreline. Here, we test the role of selection in maintaining variation among these beach mouse subspecies at multiple levels—phenotype, genotype and the environments they inhabit. While all beach subspecies have light pelage, they differ significantly in colour pattern. These subspecies are also genetically distinct: pair-wise F_st-values range from 0.23 to 0.63 and levels of gene flow are low. However, we did not find a correlation between phenotypic and genetic distance. Instead, we find a significant association between the average ‘lightness’ of each subspecies and the brightness of the substrate it inhabits: the two most genetically divergent subspecies occupy the most similar habitats and have converged on phenotype, whereas the most genetically similar subspecies occupy the most different environments and have divergent phenotypes. Moreover, allelic variation at the pigmentation gene, Mc1r, is statistically correlated with these colour differences but not with variation at other genetic loci. Together, these results suggest that natural selection for camouflage—via changes in Mc1r allele frequency—contributes to pigment differentiation among beach mouse subspecies.     

Environmental stability affects phenotypic evolution in a globally distributed marine picoplankton

Marine phytoplankton can evolve rapidly when confronted with aspects of climate change because of their large population sizes and fast generation times. Despite this, the importance of environment fluctuations, a key feature of climate change, has received little attention—selection experiments with marine phytoplankton are usually carried out in stable environments and use single or few representatives of a species, genus or functional group. Here we investigate whether and by how much environmental fluctuations contribute to changes in ecologically important phytoplankton traits such as C:N ratios and cell size, and test the variability of changes in these traits within the globally distributed species Ostreococcus. We have evolved 16 physiologically distinct lineages of Ostreococcus at stable high CO₂ (1031±87 μatm CO₂, SH) and fluctuating high CO₂ (1012±244 μatm CO₂, FH) for 400 generations. We find that although both fluctuation and high CO₂ drive evolution, FH-evolved lineages are smaller, have reduced C:N ratios and respond more strongly to further increases in CO₂ than do SH-evolved lineages. This indicates that environmental fluctuations are an important factor to consider when predicting how the characteristics of future phytoplankton populations will have an impact on biogeochemical cycles and higher trophic levels in marine food webs.     

Seasonal variation of genotypes and reproductive plasticity in a facultative clonal freshwater invertebrate animal (Hydra oligactis) living in a temperate lake

Facultative sexual organisms combine sexual and asexual reproduction within a single life cycle, often switching between reproductive modes depending on environmental conditions. These organisms frequently inhabit variable seasonal environments, where favorable periods alternate with unfavorable periods, generating temporally varying selection pressures that strongly influence life history decisions and hence population dynamics. Due to the rapidly accelerating changes in our global environment today, understanding the population dynamics and genetic changes in facultative sexual populations inhabiting seasonal environments is critical to assess and prepare for additional challenges that will affect such ecosystems. In this study, we aimed at obtaining insights into the seasonal population dynamics of the facultative sexual freshwater cnidarian Hydra oligactis through a combination of restriction site‐associated sequencing (RAD‐Seq) genotyping and the collection of phenotypic data on the reproductive strategy of field‐collected hydra strains in a standard laboratory environment. We reliably detected 42 MlGs from the 121 collected hydra strains. Most of MLGs (N = 35, 83.3%) were detected in only one season. Five MLGs (11.9%) were detected in two seasons, one (2.4%) in three seasons and one (2.4%) in all four seasons. We found no significant genetic change during the 2 years in the study population. Clone lines were detected between seasons and even years, suggesting that clonal lineages can persist for a long time in a natural population. We also found that distinct genotypes differ in sexual reproduction frequency, but these differences did not affect whether genotypes reappeared across samplings. Our study provides key insights into the biology of natural hydra populations, while also contributing to understanding the population biology of facultative sexual species inhabiting freshwater ecosystems.     

Interrelationships of Meloidogyne Species with Flue-cured Tobacco

Microplot and field experiments were conducted to determine relationships of population densities of Meloidogyne spp. to performance of flue-cured tobacco. A 3-yr microplot study of these interactions involved varying initial nematode numbers (P_i).and use of ethoprop to re-establish ranges of nematode densities. Field experiments included various nematicides at different locations. Regression analyses of microplot data from a loamy sand showed that cured-leaf yield losses on ''Coker 319'' for each 10-fold increase in P_i were as follows: M. javanica and M. arenaria—-13-19%; M. incognita—5-10%; M. hapla—3.4-5%; and 3% for M. incognita on resistant ''Speight G-28'' tobacco. A P_i of 750 eggs and larvae/500 cm³ of soil of all species except M. hapla caused a significant yield loss; only large numbers of M. hapla effected a loss. M. arenaria was the most tolerant species to ethoprop. Root-gall indices for microplot and most field-nematicide tests also were correlated negatively with yield. Relationships of P_i(s) and necrosis indices to yield were best characterized by linear regression models, whereas midseason numbers of eggs plus larvae (P_m) and sometimes gall indices vs. yield were better characterized by quadratic models. The relation of field P_m and yield was also adequately described by the Seinhorst model. Degrees of root galling, root necrosis, yield losses, and basic rates of reproduction on tobacco generally increased from M. hapla to M. incognita to M. arenaria to M. javanica.     

An evolutionary maximum principle for density-dependent population dynamics in a fluctuating environment

The evolution of population dynamics in a stochastic environment is analysed under a general form of density-dependence with genetic variation in r and K, the intrinsic rate of increase and carrying capacity in the average environment, and in σ_e², the environmental variance of population growth rate. The continuous-time model assumes a large population size and a stationary distribution of environments with no autocorrelation. For a given population density, N, and genotype frequency, p, the expected selection gradient is always towards an increased population growth rate, and the expected fitness of a genotype is its Malthusian fitness in the average environment minus the covariance of its growth rate with that of the population. Long-term evolution maximizes the expected value of the density-dependence function, averaged over the stationary distribution of N. In the θ-logistic model, where density dependence of population growth is a function of N^θ, long-term evolution maximizes E[N^θ]=[1−σ_e²/(2r)]K^θ. While σ_e² is always selected to decrease, r and K are always selected to increase, implying a genetic trade-off among them. By contrast, given the other parameters, θ has an intermediate optimum between 1.781 and 2 corresponding to the limits of high or low stochasticity.     

Mycelial carton galleries of Azteca brevis (Formicidae) as a multi-species network

Apart from growing fungi for nutrition, as seen in the New World Attini, ants cultivate fungi for reinforcement of the walls of their nests or tunnel-shaped runway galleries. These fungi are grown on organic material such as bark, epiphylls or trichomes, and form stable ‘carton structures’. In this study, the carton of the runway galleries built by Azteca brevis (Formicidae, Dolichoderinae) on branches of Tetrathylacium macrophyllum (Flacourtiaceae) is investigated. For the first time, molecular tools are used to address the biodiversity and phylogenetic affinities of fungi involved in tropical ant carton architecture, a previously neglected ant–fungus mutualism.The A. brevis carton involves a complex association of several fungi. All the isolated fungi were unequivocally placed within the Chaetothyriales by DNA sequence data. Whereas five types of fungal hyphae were morphologically distinguishable, our DNA data showed that more species are involved, applying a phylogenetic species concept based on DNA phylogenies and hyphal morphology. In contrast to the New World Attini with their many-to-one (different ant species—one fungal cultivar) pattern, and temperate Lasius with a one-to-two (one ant species—two mutualists) or many-to-one (different ant species share the same mutualist) system, the A. brevis–fungi association is a one-to-many multi-species network. Vertical fungus transmission has not yet been found, indicating that the A. brevis–fungi interaction is rather generalized.     

Diatom assemblages promote ice formation in large lakes

We present evidence for the directed formation of ice by planktonic communities dominated by filamentous diatoms sampled from the ice-covered Laurentian Great Lakes. We hypothesize that ice formation promotes attachment of these non-motile phytoplankton to overlying ice, thereby maintaining a favorable position for the diatoms in the photic zone. However, it is unclear whether the diatoms themselves are responsible for ice nucleation. Scanning electron microscopy revealed associations of bacterial epiphytes with the dominant diatoms of the phytoplankton assemblage, and bacteria isolated from the phytoplankton showed elevated temperatures of crystallization (T_c) as high as −3 °C. Ice nucleation-active bacteria were identified as belonging to the genus Pseudomonas, but we could not demonstrate that they were sufficiently abundant to incite the observed freezing. Regardless of the source of ice nucleation activity, the resulting production of frazil ice may provide a means for the diatoms to be recruited to the overlying lake ice, thereby increasing their fitness. Bacterial epiphytes are likewise expected to benefit from their association with the diatoms as recipients of organic carbon excreted by their hosts. This novel mechanism illuminates a previously undescribed stage of the life cycle of the meroplanktonic diatoms that bloom in Lake Erie and other Great Lakes during winter and offers a model relevant to aquatic ecosystems having seasonal ice cover around the world.     

A new tarkadectine primate from the Eocene of Inner Mongolia,China: phylogenetic and biogeographic implications

Tarka and Tarkadectes are Middle Eocene mammals known only from the Rocky Mountains region of North America. Previous work has suggested that they are members of the Plagiomenidae, an extinct family often included in the order Dermoptera. Here we describe a new primate, Tarkops mckennai gen. et sp. nov., from the early Middle Eocene Irdinmanha Formation of Inner Mongolia, China. The new taxon is particularly similar to Tarka and Tarkadectes, but it also displays many features observed in omomyids. A phylogenetic analysis based on a data matrix including 59 taxa and 444 dental characters suggests that Tarkops, Tarka and Tarkadectes form a monophyletic group—the Tarkadectinae—that is nested within the omomyid clade. Within Omomyidae, tarkadectines appear to be closely related to Macrotarsius. Dermoptera, including extant and extinct flying lemurs and plagiomenids, is recognized as a clade nesting within the polyphyletic group of plesiadapiforms, therefore supporting the previous suggestion that the relationship between dermopterans and primates is as close as that between plesiadapiforms and primates. The distribution of tarkadectine primates on both sides of the Pacific Ocean basin suggests that palaeoenvironmental conditions appropriate to sustain primates occurred across a vast expanse of Asia and North America during the Middle Eocene.     

Vampires in the oceans: predatory cercozoan amoebae in marine habitats

Vampire amoebae (vampyrellids) are predators of algae, fungi, protozoa and small metazoans known primarily from soils and in freshwater habitats. They are among the very few heterotrophic naked, filose and reticulose protists that have received some attention from a morphological and ecological point of view over the last few decades, because of the peculiar mode of feeding of known species. Yet, the true extent of their biodiversity remains largely unknown. Here we use a complementary approach of culturing and sequence database mining to address this issue, focusing our efforts on marine environments, where vampyrellids are very poorly known. We present 10 new vampyrellid isolates, 8 from marine or brackish sediments, and 2 from soil or freshwater sediment. Two of the former correspond to the genera Thalassomyxa Grell and Penardia Cash for which sequence data were previously unavailable. Small-subunit ribosomal DNA analysis confirms they are all related to previously sequenced vampyrellids. An exhaustive screening of the NCBI GenBank database and of 454 sequence data generated by the European BioMarKs consortium revealed hundreds of distinct environmental vampyrellid sequences. We show that vampyrellids are much more diverse than previously thought, especially in marine habitats. Our new isolates, which cover almost the full phylogenetic range of vampyrellid sequences revealed in this study, offer a rare opportunity to integrate data from environmental DNA surveys with phenotypic information. However, the very large genetic diversity we highlight within vampyrellids (especially in marine sediments and soils) contrasts with the paradoxically low morphological distinctiveness we observed across our isolates.     

The oldest peracarid crustacean reveals a Late Devonian freshwater colonization by isopod relatives

Peracarida (e.g. woodlice and side-swimmers) are, together with their sister-group Eucarida (e.g. krill and decapods), the most speciose group of modern crustaceans, suggested to have appeared as early as the Ordovician. While eucarids'' incursion onto land consists of mainly freshwater and littoral grounds, some peracarids have evolved fully terrestrial ground-crawling ecologies, inhabiting even our gardens in temperate regions (e.g. pillbugs and sowbugs). Their fossil record extends back to the Carboniferous and consists mainly of marine occurrences. Here, we provide a complete re-analysis of a fossil arthropod—Oxyuropoda—reported in 1908 from the Late Devonian floodplains of Ireland, and left with unresolved systematic affinities despite a century of attempts at identification. Known from a single specimen preserved in two dimensions, we analysed its anatomy using digital microscopy and multispectral macroimaging to enhance the contrast of morphological structures. The new anatomical characters and completeness of Oxyuropoda, together with a phylogenetic analysis with representatives of all major Eumalacostraca groups, indicate that Oxyuropoda is a crown peracarid, part of a clade including amphipods and isopods. As such, Oxyuropoda is the oldest known species Peracarida, and provides evidence that derived peracarids had an incursion into freshwater and terrestrial environments as early as the Famennian, more than 360 Ma.     

Multiple genetic divergences and population expansions of a Mediterranean sandfly,Phlebotomus ariasi,in Europe during the Pleistocene glacial cycles

Phlebotomus ariasi is one of the two sandflies transmitting the causative agent of zoonotic leishmaniasis, Leishmania infantum, in France and Iberia, and provides a rare case study of the postglacial re-colonization of France by a Mediterranean species. Four DNA sequences were analysed—mitochondrial cytochrome b (cyt b), nuclear elongation factor-1α (EF-1α) and two anonymous nuclear loci—for 14–15 French populations and single populations from northeast Spain, northwest Spain, Portugal and Morocco. The presence of cryptic sibling species was not revealed by phylogenetic analyses and testing for reproductive isolation between sympatric populations defined by the two most divergent cyt b haplogroups. No locus was shown to be under positive directional or balancing selection and, therefore, molecular variation was explained demographically. Each nuclear locus showed shallow isolation by distance from Portugal to the French Pyrenees, but for both cyt b and EF-1α there was then a step change to the upland Massif Central, where leading-edge populations showed low diversity at all loci. Multiple genetic divergences and population expansions were detected by analyses of cyt b and dated to the Pleistocene. Endemicity of one cyt b sub-lineage suggested the presence of a refuge north of the Pyrenees during the last glacial period. Monopolization of the Massif Central by genetically differentiated populations of P. ariasi might possibly hinder the northwards spread of leishmaniasis.     

Changing dynamics of Caribbean reef carbonate budgets: emergence of reef bioeroders as critical controls on present and future reef growth potential

Coral cover has declined rapidly on Caribbean reefs since the early 1980s, reducing carbonate production and reef growth. Using a cross-regional dataset, we show that widespread reductions in bioerosion rates—a key carbonate cycling process—have accompanied carbonate production declines. Bioerosion by parrotfish, urchins, endolithic sponges and microendoliths collectively averages 2 G (where G = kg CaCO₃ m⁻² yr⁻¹) (range 0.96–3.67 G). This rate is at least 75% lower than that reported from Caribbean reefs prior to their shift towards their present degraded state. Despite chronic overfishing, parrotfish are the dominant bioeroders, but erosion rates are reduced from averages of approximately 4 to 1.6 G. Urchin erosion rates have declined further and are functionally irrelevant to bioerosion on most reefs. These changes demonstrate a fundamental shift in Caribbean reef carbonate budget dynamics. To-date, reduced bioerosion rates have partially offset carbonate production declines, limiting the extent to which more widespread transitions to negative budget states have occurred. However, given the poor prognosis for coral recovery in the Caribbean and reported shifts to coral community states dominated by slower calcifying taxa, a continued transition from production to bioerosion-controlled budget states, which will increasingly threaten reef growth, is predicted.