Mark A. Hixon

Fisheries Sustainability via Protection of Age Structure and Spatial Distribution of Fish Populations

Abstract Numerous groundfish stocks in both the Atlantic and Pacific are considered overfished, resulting in large-scale fishery closures. Fishing, in addition to simply removing biomass, also truncates the age and size structure of fish populations and often results in localized depletions. We summarize recent research suggesting that an old-growth age structure, combined with a broad spatial distribution of spawning and recruitment, is at least as important as spawning biomass in maintaining long-term sustainable population levels. In particular, there is evidence that older, larger female rockfishes produce larvae that withstand starvation longer and grow faster than the offspring of younger fish, that stocks may actually consist of several reproductively isolated units, and that recruitment may come from only a small and different fraction of the spawning population each year. None of these phenomena is accounted for in current management programs. We examine alternative management measures that addre...

POPULATION REGULATION: HISTORICAL CONTEXT AND CONTEMPORARY CHALLENGES OF OPEN VS. CLOSED SYSTEMS

By definition, a population is regulated if it persists for many generations with fluctuations bounded above zero with high probability. Regulation thus requires den- sity-dependent negative feedback whereby the population has a propensity to increase when small and decrease when large. Ultimately, extinction occurs due to regulating mechanisms becoming weaker than various disruptive events and stochastic variation. Population reg- ulation is one of the foundational concepts of ecology, yet this paradigm has often been challenged, during the first half of the 20th century when the concept was not clearly defined, and more recently by some who study demographically open populations. The history of ecology reveals that earlier manifestations of the concept focused mostly on competition as the mechanism of population regulation. Because competition is often not evident in nature, it was sometimes concluded that population regulation was therefore also absent. However, predation in the broadest sense can also cause density dependence. By the 1950s, the idea that demographic density dependence was essential (but not suffi- cient) for population regulation was well established, and since then, challenges to the general concept have been short lived. However, some now believe that metapopulations composed of demographically open local populations can persist without density depen- dence. In particular, some recent manifestations of the Recruitment Limitation Hypothesis all but preclude the possibility of regulation. The theory of locally open populations indicates that persistence always relies on direct demographic density dependence at some spatial and temporal scale, even in models re- portedly demonstrating the contrary. There is also increasing empirical evidence, especially in marine systems where competition for space is not self evident, that local density de- pendence is more pervasive than previously assumed and is often caused by predation. However, there are currently insufficient data to test unequivocally whether or not any persistent metapopulation is regulated. The challenge for more complete understanding of regulation of metapopulations lies in combined empirical and theoretical studies that bridge the gap between smaller scale field experiments and larger scale phenomena that can pres- ently be explored solely by theory.

Coral Reef Fishes

About 4500 fish species inhabit coral reefs globally, yet their fisheries are overexploited, their habitat is threatened, and there are indications that species are endangered. Coral reef fishes are so diverse that there are many exceptions to virtually every generalization that can be made about them. The typical species is a distinctively colored, highly compressed perciform that readily maneuvers and picks small invertebrates from complex reef habitats. Behaviorally, mutualism, territoriality, antipredatory mechanisms, and complex social systems (sometimes involving sex reversal) are common. Reproduction is typically via broadcast spawning, with pelagic larval duration averaging about a month, and life span less than a decade. Population dynamics are apparently driven by fluctuations in larval mortality, and populations appear to be regulated in the absence of fishing by density-dependent fecundity and early postsettlement mortality via predation. Community structure is complex, involving numerous feeding guilds, and includes day–night transitions between diurnal and nocturnal assemblages. Communities are variously structured by recruitment, competition, and predation in a way that maintains high local species diversity.

No-take Reserve Networks: Sustaining Fishery Populations and Marine Ecosystems

Abstract Improved management approaches are needed to reduce the rate at which humans are depleting exploited marine populations and degrading marine ecosystems. Networks of no-take marine reserves are promising management tools because of their potential to (1) protect coastal ecosystem structure and functioning, (2) benefit exploited populations and fisheries, (3) improve scientific understanding of marine ecosystems, and (4) provide enriched opportunities for non-extractive human activities. By protecting marine ecosystems and their populations, no-take reserve networks can reduce risk by providing important insurance for fishery managers against overexploitation of individual populations. Replicated reserves also foster strong scientific testing of fishery and conservation management strategies. Reserve networks will require social acceptance, adequate enforcement, and effective scientific evaluation to be successful. Processes for reserve establishment should accommodate adaptive management so bounda...

Competition, predation, and density-dependent mortality in demersal marine fishes

The relative roles of competition and predation in demographic density dependence are poorly known. A tractable experimental design to determine such effects and their interactions for demersal (seafloor oriented) fishes and similar sedentary species is cross-factoring multiple densities of new recruits with the presence and absence of predators. This design allows one to distinguish between density-dependent mortality due to competition alone, predation alone, or an interaction between the two, especially when supplemental field observations are available. To date, 14 species of marine fish have been examined with some variant of this design, and for 12 species predation was demonstrated to be the sole or major cause of density dependence. However, as competition may be slow acting relative to predation, the importance of competition can be underestimated in short-term experiments. On the Great Barrier Reef, we conducted a long-term field experiment in which multiple densities of new recruits of a planktivorous damselfish were cross-factored with the presence or absence of resident piscivorous fish on patch reefs. During the first 10 months, no density-dependent mortality was detected, regardless of whether resident predators were present or absent. By the end of the experiment at 17 months, per capita mortality was strongly density dependent and highly compensatory in both predator treatments; all reefs ultimately supported nearly the same adult density regardless of experimental treatment. Examination of treatment effect sizes suggested that competition was the main source of density-dependent mortality, with predation being merely a proximate agent of death. We hypothesize that predators were ineffective in this system compared with similar studies elsewhere because prey density was low relative to ample prey refuges provided by highly complex corals. Combined with previous studies, these findings indicate that density-dependent mortality in demersal marine fishes is often caused by interplay of predation and competition, whose roles may be altered by variation in habitat complexity and larval supply. These conclusions are relevant to marine fisheries models, which typically assume that density dependence is due solely to intraspecific competition.

Succession and Herbivory: Effects of Differential Fish Grazing on Hawaiian Coral-Reef Algae

Most general models do not include herbivory as a major agent of successional change. Potentially, herbivores can affect succession in three ways: accelerating or decelerating the rate of succession, where the sequence of dominant species is unaltered, or deflecting succession onto a new trajectory, where the species composition of dominants becomes substantially different than during ungrazed succession. We examined these alternatives for benthic algae on a coral—reef crest off Oahu, Hawaii. In this system, exposed coral—rock surfaces naturally undergo one of two major grazing regimes: (1) relatively protected inside defended territories of the damselfish Stegastes fasciolatus (Pomacentridae), where the benthos is dominated by filamentous algae; or (2) exposed to abundant schooling parrotfishes (Scaridae) and surgeonfishes (Acanthuridae) outside territories, where the bottom is covered mostly by crustose algae. We compared the effects of this differential grazing on primary succession, relative to ungrazed succession, by distributing on the same date 1332 settling surfaces among three treatments: exposed inside damselfish territories, exposed just outside territories, and within fish—exclusion cages just outside territories. To balance the advantages and disadvantages of different settling surfaces, we used equal numbers of each of three kinds of 50—cm2 settling plates: naturally contoured coral rock, coral rock cut into flat plates, and roughly sanded PVC plastic. To follow relative successional pathways, we sampled destructively 63 plates (21 from each grazing treatment) 17 times over 1 yr. Plates placed in the field several months before and after the main experiment suggested no seasonal differences in algal colonization. A concurrent cage—control experiment involving 144 settling plates, combined with measurements of light and water motion inside vs. outside cages, indicated that the secondary effects of cages were minor compared to the primary effect of preventing fish grazing. In the absence of fish grazing within cages, algal succession over the year followed three stages: early dominance by simple green and brown filaments (such as Enteromorpha rhizoidea and Ectocarpus indicus), a midsuccessional stage dominated by thin and finely branched red filaments (such as Centroceras clavulatum and Taenioma perpusillum), and a late stage dominated by blades and coarsely branched thick filaments (especially Tolypoicladia glomerulata). Species diversity followed a unimodal pattern during ungrazed succession, declining as a few species of late—stage algae predominated. Inside damselfish territories, succession was decelerated. The early stage was protracted and the midsuccessional stage, similar to natural assemblages inside territories, still dominated by the end of the year. Here, herbivory was of moderately destructive intensity (as measured by the density of fish bite marks that removed algal holdfasts) and fairly nonselective (as measured by comparisons of the gut contents of damselfish paired with samples of their algal mats). Algal biomass reached only about a quarter of what accumulated during ungrazed succession, but species diversity gradually increased through time. By the end of the experiment, algal species diversity was greatest inside damselfish territories compared to the other two grazing treatments. Outside territories, where grazing was destructively intense, resulting in the removal of all erect algae, succession was strongly deflected. The early stage was quickly replaced by a low—biomass and low—diversity assemblage of crusts (such as Hydrolithon reinboldii) and prostrate blue—green mats (such as Calothrix crustacea), characteristic of natural assemblages outside territories. Besides demonstrating the importance of herbivory during succession and providing insight on the mechanisms involved, these patterns have ramifications for explaining the maintenance of high local species diversity on coral reefs at two spatial scales. Between patches, differential grazing by territorial damselfish vs. schooling herbivores causes succession to follow different trajectories toward different algal assemblages. Within patches defined by damselfish territories, moderate grazing decelerates succession and prolongs a high—diversity mid—successional stage. Both these patterns provide an example of predation maintaining high local diversity in tropical systems, and indicate that territorial damselfish can function as keystone species on coral reefs.

Predation effects on early post-settlement survivorship of coral-reef fishes

Little is known of the sources of mortality that affect local population dynam~cs of coralreef fishes. To examine the role of predat~on, resident p~scivorous fishes [moray eels (Muraenidae), large squirrelfishes (Holocentridae), groupers (Serranidae), and snappers (Lutjanidae)] were removed from 3 of 6 isolated patch reefs of living coral near Lee Stocking Island, Bahamas, in 1992. All 6 reefs were then seeded with natural densities of newly settled recruits of 3 species: Chromis cyanea (blue chromis, Pomacentridae), Halichoerespictus (rainbow wrasse, Labridae), and Thalassoma bifasciatum (bluehead wrasse, Labridae). Controls showed that any secondary effects of transplanting new recruits were negligible. Over the next month, survivorship of C. cyanea (mean 41.3%) and H. pictus (80.8%) on the predator-absent reefs was significantly greater than on the predator-present (control) reefs (9.4% for C. cyanea and 43.2% for H. pictus). No statistical difference was evident for T bitasciatum (48.5 vs 37.8% survival), perhaps because juveniles of this species are cleaner fish and/or because they were less conspicuous to predators than the other species. Although the size distributions of the wrasses did not differ between treatments, the size distribution of C. cyanea shifted significantly. At the end of the experiment, surviv.ing C. cyanea were slightly larger on the predator-present reefs (mode = 4.0 cm total length, TL) than on the predator-absent reefs (mode = 3.5 cm TL), despite no significant difference at the start of the experiment (mode for both treatments = 3.0 cm TL). We interpret this size shift as predators differentially consuming smaller recruits and/or surviving recruits growing faster after densities were reduced by predators. Preliminary remote video monitoring of the activity of transient p~scivores [mostly jacks (Carangidae)] over the experimental reefs suggested that such predators may regularly visit isolated reefs in search of prey. If so, transient predators may have accounted for the surprisingly low first-month survivorship (about 40 to 80%) of new recruits on reefs where resident predators were removed. In any case, we conclude that resident predators can substantially alter the local density and size structure of reef fishes shortly after they settle from the plankton. Because piscivores differentially affected the survivorship of different species, predation may also influence the structure of reef-fish communities by altering the relative abundances of prey species established at the time of settlement. K E Y WORDS: Coral-reef fishes . Predat~on . Remuitment . Size distribution . Survivorship

Ten Commandments for Ecosystem-Based Fisheries Scientists

Abstract In an effort to accelerate the ongoing paradigm shift in fisheries science from the traditional single-species mindset toward more ecosystem-based approaches, we offer the following “commandments” as action items for bridging the gap between general principles and specifie methodologies. 1. Keep a perspective that is holistic, risk-averse, and adaptive. 2. Question key assumptions, no matter how basic. 3. Maintain old-growth age structure in fish populations. 4. Characterize and maintain the natural spatial structure of fish stocks. 5. Characterize and maintain viable fish habitats. 6. Characterize and maintain ecosystem resilience. 7. Identify and maintain critical food web connections. 8. Account for ecosystem change through time. 9. Account for evolutionary change caused by fishing. 10. Implement an approach that is integrated, interdisciplinary, and inclusive. Although the shift in worldview embodied in these commandments can occur immediately without additional funding, full implementation o...

Artificial Reefs: The Importance of Comparisons with Natural Reefs

Abstract Methods used to evaluate the performance of an artificial reef will vary according to the purpose for which the reef was built. To determine how well artificial reefs mitigate losses due to human activities on natural reefs, the performance of artificial reefs should be evaluated using contemporaneous comparisons with relatively undisturbed natural reefs. Unfortunately, comparisons between artificial and natural reefs are typically confounded by differences in reef size, age, and isolation. We compared colonization and subsequent assemblage structure of reef fishes on coral and artificial (concrete block) reefs in which reef size, age, and isolation were standardized. Species richness and fish abundance (all species combined) were greater on reefs of natural rather than artificial structure, but substantial differences in species composition were not detected. Our results suggest that artificial reefs with structural complexity and other abiotic and biotic features similar to those of natural ree...

Worst case scenario: potential long-term effects of invasive predatory lionfish ( Pterois volitans ) on Atlantic and Caribbean coral-reef communities

The Pacific red lionfish has recently invaded Western Atlantic and Caribbean coral reefs, and may become one of the most ecologically harmful marine fish introductions to date. Lionfish possess a broad suite of traits that makes them particularly successful invaders and strong negative interactors with native fauna, including defensive venomous spines, cryptic form, color and behavior, habitat generality, high competitive ability, low parasite load, efficient predation, rapid growth, and high reproductive rates. With an eye on the future, we describe a possible “worst case scenario” in which the direct and indirect effects of lionfish could combine with the impacts of preexisting stressors—especially overfishing—and cause substantial deleterious changes in coral-reef communities. We also discuss management actions that could be taken to minimize these potential effects by, first, developing targeted lionfish fisheries and local removals, and second, enhancing native biotic resistance, particularly via marine reserves that could conserve and foster potential natural enemies of this invader. Ultimately, the lionfish invasion will be limited either by the lionfish starving—the worst end to the worst case scenario—or by some combination of native pathogens, parasites, predators, and competitors controlling the abundance of lionfish.