Robert R. Warner

ENVIRONMENTAL VARIABILITY PROMOTES COEXISTENCE IN LOTTERY COMPETITIVE SYSTEMS

In deterministic approaches to modeling, two species are generally regarded as capable of coexistence if the model has a stable equilibrium with both species in positive numbers. Temporal environmental variability is assumed to reduce the likelihood of coexistence by keeping species abundances away from equilibrium. Here we present a contrasting view based on a model of competition for space among coral reef fishes, or any similarly territorial animals. The model has no stable equilibrium point with both species in positive abundance, yet both species persist in the system provided environmental variability in birth rates is sufficiently high. In general the higher the environmental variability the more likely it is that coexistence will occur. This conclusion is not affected by one species having a mean advantage over the other. Not all kinds of environmental variability necessarily lead to coexistence, however, for when the death rates of the two species are highly variable and negatively correlated, the extinction of one species, determined by chance, is likely to occur. The results in this paper are shown to depend on the nonlinearity of the dynamics of the system. This nonlinearity arises from the simple fact that the animals have overlapping generations. When applied to the coral reef fish setting, our analysis confirms the view that coexistence can occur in a system where space is allocated largely at random, provided environmental variability is sufficiently great (Sale 1977); but our explanations and predictions differ in detail with those of Sale.

Coexistence Mediated by Recruitment Fluctuations: A Field Guide to the Storage Effect

For most species, a changeable environment creates a situation in which recruitment varies considerably from one breeding season to the next. If adults survive well, an occasional favorable recruitment can sustain population numbers over long periods. In effect, the gains made in favorable periods are stored in the adult population. Storage is particularly important when the species is at low densities, because then the potential population growth rate is very high if a favorable period occurs. Our past work showed that the storage mechanism could lead to coexistence of two species in lottery competition for space, as long as generations overlapped and there was sufficient variation in recruitment (Chesson and Warner 1981). This was true even if one species had an average competitive advantage. The storage model also operates when more than two species are competing, when resources renew independently of population sizes, and when not all the resource is used. It also operates in simple Lotka-Volterra systems in which adults do not compete directly with juveniles. The field ecologist is faced with the more practical problem of determining whether the storage mechanism is operating in a particular system. Species with relatively long lives and high fecundities are most likely to enjoy the benefits of the storage effect. Environments that theoretically elicit these life history characteristics are relatively benign and permanent for established adults, but are such that births and/or juvenile survivorship vary widely. Trees and many marine organisms are examples of species with the proper life histories, and storage may be important in maintaining the high diversity of these communities. The storage mechanism is capable of independently maintaining species coexistence, and we provide some suggestions on how to distinguish qualitatively the operation of storage from alternative mechanisms. We expect, however, that storage will make some positive contribution toward species persistence in nearly all communities, and we give a method for estimating empirically how large that contribution is.

ECOLOGICAL CRITERIA FOR EVALUATING CANDIDATE SITES FOR MARINE RESERVES

Several schemes have been developed to help select the locations of marine reserves. All of them combine social, economic, and biological criteria, and few offer any guidance as to how to prioritize among the criteria identified. This can imply that the relative weights given to different criteria are unimportant. Where two sites are of equal value ecologically; then socioeconomic criteria should dominate the choice of which should be protected. However, in many cases, socioeconomic criteria are given equal or greater weight than ecological considerations in the choice of sites. This can lead to selection of reserves with little biological value that fail to meet many of the desired objectives. To avoid such a possibility, we develop a series of criteria that allow preliminary evaluation of candidate sites according to their relative biological values in advance of the application of socioeconomic criteria. We include criteria that,. while not strictly biological, have a strong influence on the species present or ecological processes. Out scheme enables sites to be assessed according to their biodiversity, the processes which underpin that diversity, and the processes that support fisheries and provide a spectrum of other services important to people. Criteria that capture biodiversity values include biogeographic representation, habitat representation and heterogeneity, and presence of species or populations of special interest (e.g., threatened species). Criteria that capture sustainability of biodiversity and fishery values include the size of reserves necessary to protect viable habitats, presence of exploitable species, vulnerable life stages, connectivity among reserves, links among ecosystems, and provision of ecosystem services to people. Criteria measuring human and natural threats enable candidate sites to be eliminated from consideration if risks are too great, but also help prioritize among sites where threats can be mitigated by protection. While our criteria can be applied to the design of reserve networks, they also enable choice of single reserves to be made in the context of the attributes of existing protected areas. The overall goal of our scheme is to promote the development of reserve networks that will maintain biodiversity and ecosystem functioning at large scales. The values of eco-system goods and services for people ultimately depend on meeting this objective.

The Adaptive Significance of Sequential Hermaphroditism in Animals

In some cases, sequential hermaphroditism can convey a selective advantage to an individual by increasing its reproductive potential relative to nontransforming members of the population. This is because age-specific fecundity in many populations is not distributed in the same way for males and females. By functioning as that sex which has the higher fecundity in a particular age span, an individual could increase its reproductive potential relative to lifetime males or females. The magnitude of the reward that comes from such sex changes depends on both the demography of the population and its spawning habits. Protandry may be selected for in populations where female fecundity increases with age and where individuals mate at random. Factors which favor the evolution of protogyny are those which tend to depress male fecundity values at early ages, such as inexperience, territoriality, or female mate selection. Selection for protogyny can also exist when female fecundity decreases with age, although this situation seems rare in the field. It appears that the nature of the fecundity schedule for females has a greater effect on the magnitude of the selection pressure for sequential hermaphroditism than does the age structure of the population. If sequential hermaphroditism becomes genetically fixed in some members of a population with differential age-specific fecundities, the frequency of the hermaphrodites should increase over time until they eliminate the gonochoristic individuals. The pattern of sexual transformation eventually reached in a population is predictable through the use of a simulation model developed here. The pattern depends on the age structure, female fecundity schedule, and mating characteristics of the population. For two examples, the predictions appear consistent with what is seen in nature. At equilibrium, the simulated populations consist of individuals which changed sex at one of two ages, and each type has essentially the same reproductive potential. This suggests that we should see a rather sharp break in age-specific sex ratios in protogynous or protandrous populations. Some hermaphroditic populations exhibit such sharp changes, but others do not. The expected pattern would tend to be obscured by differing growth rates among individuals.

Sex change and sexual selection.

Many writers have discussed sequential hermaphroditism, wherein individuals are all born of one sex and change to the other as they grow older, in terms of its advantage to the species (1). Ghiselin (2) shifted the focus by suggesting that if members of one sex increase in fertility more rapidly with age than those of the other, then natural selection will favor a genotype whose individuals are all born into the sex that suffers less from being young (the sex whose fertility increases

Marine defaunation: Animal loss in the global ocean

Marine animals are disappearing, too The loss of animal species in terrestrial environments has been well documented and is continuing. Loss of species in marine environments has been slower than in terrestrial systems, but appears to be increasing rapidly. McCauley et al. review the recent patterns of species decline and loss in marine environments. Though they note many worrying declines, they also highlight approaches that might allow us to prevent the type of massive defaunation that has occurred on land. Science, this issue 10.1126/science.1255641 BACKGROUND Comparing patterns of terrestrial and marine defaunation helps to place human impacts on marine fauna in context and to navigate toward recovery. Defaunation began in earnest tens of thousands of years later in the oceans than it did on land. Although defaunation has been less severe in the oceans than on land, our effects on marine animals are increasing in pace and impact. Humans have caused few complete extinctions in the sea, but we are responsible for many ecological, commercial, and local extinctions. Despite our late start, humans have already powerfully changed virtually all major marine ecosystems. ADVANCES Humans have profoundly decreased the abundance of both large (e.g., whales) and small (e.g., anchovies) marine fauna. Such declines can generate waves of ecological change that travel both up and down marine food webs and can alter ocean ecosystem functioning. Human harvesters have also been a major force of evolutionary change in the oceans and have reshaped the genetic structure of marine animal populations. Climate change threatens to accelerate marine defaunation over the next century. The high mobility of many marine animals offers some increased, though limited, capacity for marine species to respond to climate stress, but it also exposes many species to increased risk from other stressors. Because humans are intensely reliant on ocean ecosystems for food and other ecosystem services, we are deeply affected by all of these forecasted changes. Three lessons emerge when comparing the marine and terrestrial defaunation experiences: (i) today’s low rates of marine extinction may be the prelude to a major extinction pulse, similar to that observed on land during the industrial revolution, as the footprint of human ocean use widens; (ii) effectively slowing ocean defaunation requires both protected areas and careful management of the intervening ocean matrix; and (iii) the terrestrial experience and current trends in ocean use suggest that habitat destruction is likely to become an increasingly dominant threat to ocean wildlife over the next 150 years. OUTLOOK Wildlife populations in the oceans have been badly damaged by human activity. Nevertheless, marine fauna generally are in better condition than terrestrial fauna: Fewer marine animal extinctions have occurred; many geographic ranges have shrunk less; and numerous ocean ecosystems remain more wild than terrestrial ecosystems. Consequently, meaningful rehabilitation of affected marine animal populations remains within the reach of managers. Human dependency on marine wildlife and the linked fate of marine and terrestrial fauna necessitate that we act quickly to slow the advance of marine defaunation. Timeline (log scale) of marine and terrestrial defaunation. The marine defaunation experience is much less advanced, even though humans have been harvesting ocean wildlife for thousands of years. The recent industrialization of this harvest, however, initiated an era of intense marine wildlife declines. If left unmanaged, we predict that marine habitat alteration, along with climate change (colored bar: IPCC warming), will exacerbate marine defaunation. Marine defaunation, or human-caused animal loss in the oceans, emerged forcefully only hundreds of years ago, whereas terrestrial defaunation has been occurring far longer. Though humans have caused few global marine extinctions, we have profoundly affected marine wildlife, altering the functioning and provisioning of services in every ocean. Current ocean trends, coupled with terrestrial defaunation lessons, suggest that marine defaunation rates will rapidly intensify as human use of the oceans industrializes. Though protected areas are a powerful tool to harness ocean productivity, especially when designed with future climate in mind, additional management strategies will be required. Overall, habitat degradation is likely to intensify as a major driver of marine wildlife loss. Proactive intervention can avert a marine defaunation disaster of the magnitude observed on land.

APPLYING ECOLOGICAL CRITERIA TO MARINE RESERVE DESIGN: A CASE STUDY FROM THE CALIFORNIA CHANNEL ISLANDS

Using ecological criteria as a theoretical framework, we describe the steps involved in designing a network of marine reserves for conservation and fisheries man- agement. Although we describe the case study of the Channel Islands, the approach to marine reserve design may be effective in other regions where traditional management alone does not sustain marine resources. A group of agencies, organizations, and individuals established clear goals for marine reserves in the Channel Islands, including conservation of ecosystem biodiversity, sustainable fisheries, economic viability, natural and cultural heritage, and education. Given the constraints of risk management, experimental design, monitoring, and enforcement, scientists recommended at least one, but no more than four, reserves in each biogeographic region. In general, the percentage of an area to be included in a reserve network depends on the goals. In the Channel Islands, after consideration of both conservation goals and the risk from human threats and natural catastrophes, scientists recommended reserving an area of 30-50% of all representative habitats in each biogeo- graphic region. For most species of concern, except pinnipeds and seabirds, information about distributions, dispersal, and population growth was limited. As an alternative to species distribution information, suitable habitats for species of concern were used to locate potential reserve sites. We used a simulated annealing algorithm to identify potential reserve network scenarios that would represent all habitats within the smallest area possible. The analysis produced an array of potential reserve network scenarios that all met the established

Application of ecological criteria in selecting marine reserves and developing reserve networks

Marine reserves are being established worldwide in response to a growing recognition of the conservation crisis that is building in the oceans. However, designation of reserves has been largely opportunistic, or protective measures have been implemented (often overlapping and sometimes in conflict) by different entities seeking to achieve dif- ferent ends. This has created confusion among both users and enforcers, and the proliferation of different measures provides a false sense of protection where little is offered. This paper sets out a procedure grounded in current understanding of ecological processes, that allows the evaluation and selection of reserve sites in order to develop functional, interconnected networks of fully protected reserves that will fulfill multiple objectives. By fully protected we mean permanently closed to fishing and other resource extraction. We provide a frame- work that unifies the central aims of conservation and fishery management, while also meeting other human needs such as the provision of ecosystem services (e.g., maintenance of coastal water quality, shoreline protection, and recreational opportunities). In our scheme, candidate sites for reserves are evaluated against 12 criteria focused toward sustaining the biological integrity and productivity of marine systems at both local and regional scales. While a limited number of sites will be indispensable in a network, many will be of similar value as reserves, allowing the design of numerous alternative, biologically adequate net- works. Devising multiple network designs will help ensure that ecological functionality is preserved throughout the socioeconomic evaluation process. Too often, socioeconomic cri- teria have dominated the process of reserve selection, potentially undermining their efficacy. We argue that application of biological criteria must precede and inform socioeconomic evaluation, since maintenance of ecosystem functioning is essential for meeting all of the goals for reserves. It is critical that stakeholders are fully involved throughout this process. Application of the proposed criteria will lead to networks whose multifunctionality will help unite the objectives of different management entities, so accelerating progress toward improved stewardship of the oceans.

Matching marine reserve design to reserve objectives

Recent interest in using marine reserves for marine resource management and conservation has largely been driven by the hope that reserves might counteract declines in fish populations and protect the biodiversity of the seas. However, the creation of reserves has led to dissension from some interested groups, such as fishermen, who fear that reserves will do more harm than good. These perceived differences in the effect of marine reserves on various stakeholder interests has led to a contentious debate over their merit. We argue here that recent findings in marine ecology suggest that this debate is largely unnecessary, and that a single general design of a network of reserves of moderate size and variable spacing can meet the needs and goals of most stakeholders interested in marine resources.

Sexual conflict: males with highest mating success convey the lowest fertilization benefits to females

In natural populations of a coral reef fish (the bluehead wrasse, Thalassoma bifasciatum), males with the highest daily mating success produce the fewest sperm per mating, and this is reflected in significantly lower fertilization rates. The average amount released by males in pair-mating was 3.3 x 106 spermatozoa, resulting in a fertilization rate of 96%. Sperm released per spawn declined with increasing mating success, so that females mating with the most successful males had less than 93% of their eggs fertilized. It is unlikely that high mating-success males are physiologically incapable of increasing sperm production, because younger males with different mating strategies have absolutely larger testes and higher daily sperm output. Feeding experiments suggest that high-success males are diverting energy from gamete production to other fitness-enhancing activities such as mate guarding. Females incur the cost of low sperm release by having fewer of their eggs fertilized. There are no obvious compensatory benefits to females from mating with high-success males.