Mechanisms of coexistence in diverse herbivore–carnivore assemblages: demographic,temporal and spatial heterogeneities affecting prey vulnerability

Simple models coupling the dynamics of single predators to single prey populations tend to generate oscillatory dynamics of both predator and prey, or extirpation of the prey followed by that of the predator. In reality, such oscillatory dynamics may be counteracted by prey refugia or by opportunities for prey switching by the predator in multi‐prey assemblages. How these mechanisms operate depends on relative prey vulnerability, a factor ignored in simple interactive models. I outline how compositional, temporal, demographic and spatial heterogeneities help explain the contrasting effects of top predators on large herbivore abundance and population dynamics in species‐rich African savanna ecosystems compared with less species‐diverse northern temperate or subarctic ecosystems. Demographically, mortality inflicted by predation depends on the relative size and life history stage of the prey. Because all animals eventually die and are consumed by various carnivores, the additive component of the mortality inflicted is somewhat less than the predation rate. Prey vulnerability varies annually and seasonally, and between day and night. Spatial variation in the risk of predation depends on vegetation cover as well as on the availability of food resources. During times of food shortage, herbivores become prompted to occupy more risky habitats retaining more food. Predator concentrations dependent on the abundance of primary prey species may restrict the occurrence of other potential prey species less resistant to predation. The presence of multiple herbivore species of similar size in African savannas allows the top predator, the lion, to shift its prey selection flexibly dependent on changing prey vulnerability. Hence top–down and bottom–up influences on herbivore populations are intrinsically entangled. Models coupling the population dynamics of predators and prey need to accommodate the changing influences of prey demography, temporal variation in environmental conditions, and spatial variation in the relative vulnerability of alternative prey species to predation. Synthesis While re‐established predators have had major impacts on prey populations in northern temperate regions, multiple large herbivore species typically coexist along with diverse carnivores in African savanna ecosystems. In order to explain these contrasting outcomes, certain functional heterogeneities must be recognised, including relative vulnerability of alternative prey, temporal variation in the risk of predation, demographic differences in susceptibility to predation, and spatial contrasts in exposure to predation. Food shortfalls prompt herbivores to exploit more risky habitats, meaning that top–down and bottom–up influences on prey populations are intrinsically entangled. Models coupling the interactive dynamics of predator and prey populations need to incorporate these varying influences on relative prey vulnerability.     

海州湾5种关键饵料生物的主要捕食者及其捕食压力

为了解海州湾关键饵料生物在食物网中的被捕食压力及自然死亡率波动情况,研究基于2011和2013—2020年在海州湾及其邻近海域进行的渔业资源底拖网调查资料和胃含物分析数据,以物种间的营养联系为基础,选择细螯虾(Leptochela gracilis)、日本鼓虾(Alpheus japonicus)、枪乌贼(Loligo sp.)、小黄鱼(Larimichthys polyactis)和口虾蛄(Oratosquilla oratoria)5种关键饵料生物为研究对象,通过计算捕食压力指数(Predation pressure index, PPI),分析它们在海州湾食物网中的主要捕食者及其捕食压力,并计算了纳入捕食压力指数的自然死亡系数。结果表明,细螯虾的捕食者对其年平均捕食压力指数最高,小黄鱼的捕食者对其年平均捕食压力指数最低。小眼绿鳍鱼(Chelidonichthys kumu)对细螯虾和枪乌贼的年平均捕食压力指数最高,分别为168.89和75.77;(Miichthys miiuy)对日本鼓虾和口虾蛄的年平均捕食压力指数最高,分别为39.41和9.85;海鳗(Muraenesox c...     

Vulnerability of marine forage fishes to piscivory: effects of prey behavior on susceptibility to attack and capture

We conducted a series of size-structured laboratory experiments to quantify and compare the susceptibility of several estuarine and marine forage fishes to attack and capture by piscivorous predators. Size-dependent estimates of capture success, handling time, and prey profitability were generated from single-species experiments offering bay anchovy, Atlantic menhaden, Atlantic silverside, and age-0 striped bass to piscivores. Bay anchovy and Atlantic menhaden were most susceptible to capture and yielded high profitability compared to Atlantic silverside and age-0 striped bass prey. Variation in capture success among forage species was particularly influential in generating disparate profitability functions. Although morphological differences among forage species contributed to variation in susceptibility to predation, behavioral analyses indicated that variable reaction distances to approaching predators and activity levels of prey may explain a large fraction of the observed differences in susceptibility. When several forage species were offered to predators simultaneously in larger enclosures, mortality was highest and occurred earlier for bay anchovy and Atlantic menhaden compared to other prey, which points to the strong influence of predator capture success on overall forage fish vulnerability. Our results demonstrate species-specific differences among forage fishes in the ability to avoid attack and capture by piscivores, and we conclude that the expression of antipredator behaviors contributes significantly to variation in forage species vulnerability.     

Predation on northern shrimp (Pandalus borealis) by three gadoid species

Northern shrimp (Pandalus borealis) is targeted by commercial fisheries, but is also an important prey in the marine food web. In this study, stomach content data were used to study predation on shrimp by three gadoid species, cod (Gadus morhua), haddock (Melanogrammus aeglefinus) and whiting (Merlangius merlangus), in six inshore areas around Iceland. The results showed that shrimp was more important in the diet of cod compared with the other two predators. However, the overall predation pressure was similar for cod and haddock due to the high abundance of haddock. Therefore, even though shrimp is not the primary source of food for haddock, this species can have a substantial effect on shrimp stocks when haddock abundance is high. In addition, while cod and haddock did not select for any particular size of shrimp, whiting seemed to preferentially target juvenile shrimp. The results suggest that due to the overall effects of these three predators on shrimp stocks, gadoids need to be included in the management of shrimp stocks as predation is one of the major drivers in the development of this important prey stock.     

Interactions between northern shrimp, Pandalus borealis (Pandalidae), and its key predators within the eastern Newfoundland and Labrador marine ecosystem

An examination of population trends for northern shrimp (Pandalus borealis) and its key predators off eastern Newfoundland and Labrador provided the basis for investigating predator-prey relationships within an ecosystem that experienced major changes in species composition during the 1980s and 1990s. Populations of several demersal fish species, known to feed on northern shrimp, declined to historically low levels by the early 1990s and remained depressed thereafter. Some declines were precipitous from the late 1980s to early 1990s, coincident with an increase in shrimp. Populations of other important predator species increased throughout the 1990s along with shrimp. Lacking representative estimates of shrimp consumption, the net effect on predation mortality was unquantifiable and it was not possible to demonstrate with certainty that the major increase in shrimp biomass that occurred throughout the 1990s resulted from a concomitant reduction in predation mortality. Factors (and their interactions) relevant to the dynamics of shrimp populations include the effects of ocean climate, predation, competition, as well as commercial harvesting.     

Evaluating the effects of large marine predators on mobile prey behavior across subtropical reef ecosystems

The indirect effect of predators on prey behavior, recruitment, and spatial relationships continues to attract considerable attention. However, top predators like sharks or large, mobile teleosts, which can have substantial top–down effects in ecosystems, are often difficult to study due to their large size and mobility. This has created a knowledge gap in understanding how they affect their prey through nonconsumptive effects. Here, we investigated how different functional groups of predators affected potential prey fish populations across various habitats within Biscayne Bay, FL. Using baited remote underwater videos (BRUVs), we quantified predator abundance and activity as a rough proxy for predation risk and analyzed key prey behaviors across coral reef, sea fan, seagrass, and sandy habitats. Both predator abundance and prey arrival times to the bait were strongly influenced by habitat type, with open homogenous habitats receiving faster arrival times by prey. Other prey behaviors, such as residency and risk‐associated behaviors, were potentially driven by predator interaction. Our data suggest that small predators across functional groups do not have large controlling effects on prey behavior or stress responses over short temporal scales; however, habitats where predators are more unpredictable in their occurrence (i.e., open areas) may trigger risk‐associated behaviors such as avoidance and vigilance. Our data shed new light on the importance of habitat and context for understanding how marine predators may influence prey behaviors in marine ecosystems.     

Harbour porpoises respond to climate change

The effects of climate change on marine ecosystems and in particular on marine top predators are difficult to assess due to, among other things, spatial variability, and lack of clear delineation of marine habitats. The banks of West Greenland are located in a climate sensitive area and are likely to elicit pronounced responses to oceanographic changes in the North Atlantic. The recent increase in sea temperatures on the banks of West Greenland has had cascading effects on sea ice coverage, residency of top predators, and abundance of important prey species like Atlantic cod (Gadus morhua). Here, we report on the response of one of the top predators in West Greenland; the harbour porpoise (Phocoena phocoena). The porpoises depend on locating high densities of prey species with high nutritive value and they have apparently responded to the general warming on the banks of West Greenland by longer residence times, increased consumption of Atlantic cod resulting in improved body condition in the form of larger fat deposits in blubber, compared to the situation during a cold period in the 1990s. This is one of the few examples of a measurable effect of climate change on a marine mammal population.     

Implications of a fluctuating fish predator guild on behavior, distribution, and abundance of a shared prey species: the grass shrimp Palaemonetes pugio

In some systems, the identity of a prey species' dominant predator(s) may not be constant over time. In cases in which a prey species exhibits different responses to various predator species, such changes in predator identity may have population-wide consequences. Our goals were to determine (1) whether mortality of and refuge use by the grass shrimp, Palaemonetes pugio, were predator-specific, and (2) how effects of prey size and habitat interacted with predator type. Striped bass (Morone saxatilis) exerted twice as much predation pressure as mummichog (Fundulus heteroclitus), although not equally as great on large (female) and small (male) shrimp. Mummichog, which fed preferentially on large shrimp, forced a partitioning of habitat between the two shrimp size classes. In contrast, large and small shrimp occupied similar habitats when subjected to striped bass, which fed on both size classes equally. Refuge use of grass shrimp depended on predator type. In the presence of mummichog, which occupied shallower depths in the water column than striped bass, shrimp stayed deep and close to structural habitat. Striped bass, which were deeper, caused shrimp to move high in the water column away from structural habitat. When both predators were present, shrimp distribution was similar to that when only striped bass were present, striped bass predation rate was enhanced, and overall mortality was higher than with either predator alone. Results suggest that at times when mummichogs are the dominant predators, large (female) shrimp experience higher predation than small (male) shrimp and are physically separated from their potential mates. When striped bass are more abundant, male and female shrimp may share a similar, shallow, less structure-oriented distribution and be subjected to higher mortality. When both predators are present, mortality rates may be higher still. This predator-, size-, and habitat-specificity of grass shrimp behavior suggests significant population and distribution consequences of fluctuating predator guilds and fluctuating cover of structural habitats in the field.     

Vertebrate exploitation of pulsed marine prey: a review and the example of spawning herring

Short-term bursts of prey availability occur in many ecosystems and have potential important consequences for both predator biology and ecosystem function. Examples of prey ‘pulses’ in marine ecosystems include spawning runs of several anadromous and marine fishes, horseshoe crab spawning, and salmonid juvenile outmigrations, which are exploited by numerous species of vertebrate predators. In a few cases, the fitness or demographic consequences of such predator–prey interactions are known or inferred, but too often that information remains unknown. We explored the extent of temporal and spatial variation in one example of a pulsed marine resource: the spawning of Pacific herring (Clupea pallasii). Spawning herring provide a rich, aggregated resource to which dozens of species of vertebrate predators often exhibit strong numerical responses. However, the spawning events are often variable in both time (annual differences of several to many weeks) and space (both regional and more local differences in size and timing of events). Such variability must affect more mobile predators less than area-restricted predators, and thus its effect would vary not only among species but also within species, depending on constraints of the predator life history. Unpredictability of the prey concentrations, whatever their proximate causes, may contribute to maintenance of metapopulations of prey such as herring, if unpredictability lessens the impact of predation.     

Is there safety‐in‐numbers for prey?

The abundance of prey affects the rate of predation, but little consensus exists on whether this enhances or reduces per capita mortality. Studies of aggregating prey in marine habitats generally emphasise that the probability of predation of any individual is the reciprocal of the number of prey within a school. A field experiment tested the alternative hypotheses that predation by predatory fish on schooling prey (1) increased with an increase in the number of prey per school and that this caused (2) survival to be lower in schools with more individuals. The number of prey (juvenile Acanthochromis polyacanthus ) per school was manipulated in replicate treatments with natural densities of large predatory fish (open plots) and treatments without large predatory fish (exclusion cages). Large predatory fish preyed on juveniles in a density-dependent manner and this was the key source of density-dependent mortality in plots open to all predators. There was some suggestion that small predatory fish also prey on juveniles in a density-dependent manner, but this was weak and did not translate into density-dependent mortality of juveniles. It would appear that aggregation of prey may be a successful strategy against predation from some predators, but not always every predator, or all predators in combination.     

Fish predation on juvenile brown shrimp, Penaeus aztecus Ives: The effect of simulated Spartina structure on predation rates

The effect of artificial Spartina structure on the predation rates of four estuarine fish on juvenile brown shrimp (Penaeus aztecus Ives) was examined under laboratory conditions. Vegetative structure reduced predation rates of pinfish and Atlantic croaker but did not affect predation rates of red drum and speckled trout. Pinfish and Atlantic croaker were inefficient predators, needing several strikes before successfully capturing prey. This inefficiency, necessitating repeated detection of prey organisms, probably contributed to the reduced predation rates by these fish in vegetated treatments. Although pinfish and speckled trout appeared to be strictly visual feeders, Atlantic croaker and red drum could apparently detect and feed upon shrimp through other sensory mechanisms. Differences in the mode of feeding among the fish, however, did not appear to be related to the effect of vegetative structure on predation rates. Over all of the experiments, predation rates on shrimp (50–69 mm) ranged between ≈2 and 13 shrimp·fish^?1·day^?1, and there was a positive relationship between the number of shrimp eaten and the size of the predator.     

Top–down limits on prey populations may be more severe in larger prey species,despite having fewer predators

Variation in the vulnerability of herbivore prey to predation is linked to body size, yet whether this relationship is size‐nested or size‐partitioned remains debated. If size‐partitioned, predators would be focused on prey within their preferred prey size range. If size‐nested, smaller prey species should become increasingly more vulnerable because increasingly more predators are capable of catching them. Yet, whether either of these strategies manifests in top–down prey population limitation would depend both on the number of potential predator species as well as the total mortality imposed. Here we use a rare ecosystem scale ‘natural experiment’ comparing prey population dynamics between a period of intense predator persecution and hence low predator densities and a period of active predator protection and population recovery. We use three decades of data on herbivore abundance and distribution to test the role of predation as a mechanism of population limitation among prey species that vary widely in body size. Notably, we test this within one of the few remaining systems where a near‐full suite of megaherbivores occur in high density and are thus able to include a thirtyfold range in herbivore body size gradient. We test whether top–down limitation on prey species of particular body size leads to compositional shifts in the mammalian herbivore community. Our results support both size‐nested and size‐partitioning predation but suggest that the relative top–down limiting impact on prey populations may be more severe for intermediate sized species, despite having fewer predators than small species. In addition we show that the gradual recovery of predator populations shifted the herbivore community assemblage towards large‐bodied species and has led to a community that is strongly dominated by large herbivore biomass.     

Small cryptopredators contribute to high predation rates on coral reefs

Small fishes suffer high mortality rates on coral reefs, primarily due to predation. Although studies have identified the predators of early post-settlement fishes, the predators of small cryptobenthic fishes remain largely unknown. We therefore used a series of mesocosm experiments with natural habitat and cryptobenthic fish communities to identify the impacts of a range of small potential predators, including several invertebrates, on prey fish populations. While there was high variability in predation rates, many members of the cryptobenthic fish community act as facultative cryptopredators, being prey when small and piscivores when larger. Surprisingly, we also found that smashing mantis shrimps may be important fish predators. Our results highlight the diversity of the predatory community on coral reefs and identify previously unknown trophic links in these complex ecosystems.

     

Facilitation of fisheries by natural predators depends on life history of shared prey

Predators commonly share prey with human exploiters, intuitively suggesting that there is an inherent human–predator conflict through competition for prey. Here we studied the effects of fishing and predation mortality on biomass distributions and yields of shared prey using a size‐structured model of competing populations, describing the life histories of Baltic Sea sprat and herring. Whereas both species responded in a similar fashion to increased fishing mortality, with decreasing juvenile and adult biomasses, we found that responses to predation mortality differed between species. Sprat only display weak compensatory responses with increasing predation mortality, while over a substantial range of mortalities there was a strong increase in adult (and total) herring biomass, i.e. overcompensation. The observed biomass overcompensation results from relaxed intraspecific competition as predation mortality increased, allowing for faster individual growth rates that in turn lead to a change in population composition (juvenile:adult biomass ratio). Our results suggest that the potential for biomass overcompensation is higher for species exhibiting substantial growth after maturation. Differences in size‐selectivity of predators and fishing mortality resulted in a positive effect of predation mortality on fisheries yields, which can be explained by an overcompensatory response in adult herring biomass. Thus, somewhat counter intuitive, our results suggest that fishermen, depending on prey life history, may actually benefit from allowing for a higher abundance of predators, despite competing for shared prey.     

Status of the Nemertea as predators in marine ecosystems

The ecology of nemertean predators in marine ecosystems is reviewed. Nemerteans occur in most marine environments although usually in low abundances. Some species, particularly in intertidal habitats, may reach locally high densities. During specific time periods appropriate for hunting, nemerteans roam about in search of prey. Upon receiving a stimulus (usually chemical cues), many nemertean species actively pursue their prey and follow them into their dwellings or in their tracks. Other species (many hoplonemerteans) adopt a sit-and-wait strategy, awaiting prey items in strategic locations. Nemerteans possess potent neurotoxins, killing even highly mobile prey species within a few seconds and within the activity range of its attacker. Most nemertean species prey on live marine invertebrates, but some also gather on recently dead organisms to feed on them. Heteronemerteans preferentially feed on polychaetes, while most hoplonemerteans prey on small crustaceans. The species examined to date show strong preferences for selected prey species, but will attack a variety of alternative prey organisms when deprived of their favourite species. Ontogenetic changes in prey selection appear to occur, but no further information about, e.g. size selection, is available. Feeding rates as revealed from short-term laboratory experiments range on the order of 1–5 prey items d^–1. These values apparently are overestimates, since long-term experiments report substantially lower values (0.05–0.3 prey items d^–1). Nemerteans have been reported to exert a strong impact on the population size of their prey organisms through their predation activity. Considering low predation rates, these effects may primarily be a result of indirect and additive interactions. We propose future investigations on these interactive effects in combination with other predators. Another main avenue of nemertean ecological research appears to be the examination of their role in highly structured habitats such as intertidal rocky shore and coral reef environments.     

Effects of alternative prey on predation by small mammals on gypsy moth pupae

Previous work shows that predation by small mammals is a dominant cause of mortality of low-density gypsy moths in North America and that declines in small mammal density result in increases in gypsy moth density. Here we examined whether predation by small mammals is density dependent by way of a type III functional response, and how predation is influenced by alternative prey. First we showed that the preference of predators for gypsy moth pupae was low compared to other experimental prey items, such as mealworm pupae and sunflower seeds. Predation on gypsy moth pupae was characterized by a type II functional response with percent predation highest at the lowest prey densities, whereas the functional response to sunflower seeds was characterized by a type III functional response in which predation increased with increasing prey density. These results suggest that predation by small mammals is unlikely to stabilize low-density gypsy moth populations.     

Predator diversity and density affect levels of predation upon strongly interactive species in temperate rocky reefs

Indirect effects of predators in the classic trophic cascade theory involve the effects of basal species (e.g. primary producers) mediated by predation upon strongly interactive consumers (e.g. grazers). The diversity and density of predators, and the way in which they interact, determine whether and how the effects of different predators on prey combine. Intraguild predation, for instance, was observed to dampen the effects of predators on prey in many ecosystems. In marine systems, species at high trophic levels are particularly susceptible to extinction (at least functionally). The loss of such species, which is mainly attributed to human activities (mostly fishing), is presently decreasing the diversity of marine predators in many areas of the world. Experimental studies that manipulate predator diversity and investigate the effects of this on strongly interactive consumers (i.e. those potentially capable of causing community-wide effects) in marine systems are scant, especially in the rocky sublittoral. I established an experiment that utilised cage enclosures to test whether the diversity and density of fish predators (two sea breams and two wrasses) would affect predation upon juvenile and adult sea urchins, the most important grazers in Mediterranean sublittoral rocky reefs. Changes in species identity (with sea breams producing major effects) and density of predators affected predation upon sea urchins more than changes in species richness per se. Predation upon adult sea urchins decreased in the presence of multiple predators, probably due to interference competition between sea breams and wrasses. This study suggests that factors that influence both fish predator diversity and density in Mediterranean rocky reefs (e.g. fishing and climate change) may have the potential to affect the predators' ability to control sea urchin population density, with possible repercussions for the whole benthic community structure.     

Laboratory study of the susceptibility of hatchery reared Atlantic sturgeon (Acipenser oxyrinchus Mitchill, 1815) larvae to predation

The aim of the study was to determine the susceptibility to predation of Atlantic sturgeon larvae (Acipenser oxyrinchus) reared under traditional hatchery conditions. Experiments were conducted to determine whether predators would prey on Atlantic sturgeon if alternative prey was available and if the presence of substrate on the tank bottom impacted the number of Atlantic sturgeon consumed. European perch (Perca fluviatilis) was used as the predator, and the alternative prey were three‐spined stickleback (Gasterosteus aculeatus) or gudgeon (Gobio gobio). The predators and alternative prey were obtained from the wild. The mortality of sturgeon (n = 10) and alternative prey (n = 10) caused by four predators was recorded during 15 min trials. Trials with three‐spined stickleback and gudgeon as alternative prey were performed separately. Each experimental trial was repeated five times. The predators consumed significantly more Atlantic sturgeon than alternative prey in both the experimental setups when the bottom of the tank was covered with gravel and stone substrate and when there was no substrate. In trials with three‐spined stickleback the mortality of Atlantic sturgeon in both experimental setups was 94 ± 8.94%, while that of three‐spined stickleback in the setup with substrate was 20 ± 19.23%, and without substrate it was 22 ± 10.00%. European perch also consumed more Atlantic sturgeon than they did gudgeon, and the mean Atlantic sturgeon mortality in the experimental setup with substrate was 94 ± 5.48%, while for gudgeon it was 48 ± 8.37%. In the experimental setup without substrate the predators also consumed substantially more Atlantic sturgeon than gudgeon, with a mean Atlantic sturgeon mortality of 94 ± 8.94%, while for gudgeon it was 76 ± 5.48%. The study indicated that hatchery reared Atlantic sturgeon larvae are susceptible to predation by European perch. Predation could impact the survival of juvenile Atlantic sturgeon in the natural environment, and it could be one of the factors that is impeding the restoration of this species in the Baltic Sea basin.     

Biology of the Greenland shark Somniosus microcephalus

Greenland shark Somniosus microcephalus is a potentially important yet poorly studied cold-water species inhabiting the North Atlantic and Arctic Oceans. Broad-scale changes in the Arctic ecosystem as a consequence of climate change have led to increased attention on trophic dynamics and the role of potential apex predators such as S. microcephalus in the structure of Arctic marine food webs. Although Nordic and Inuit populations have caught S. microcephalus for centuries, the species is of limited commercial interest among modern industrial fisheries. Here, the limited historical information available on S. microcephalus occurrence and ecology is reviewed and new catch, biological and life-history information from the Arctic and North Atlantic Ocean region is provided. Given the considerable by-catch rates in high North Atlantic Ocean latitudes it is suggested that S. microcephalus is an abundant predator that plays an important, yet unrecognized, role in Arctic marine ecosystems. Slow growth and large pup sizes, however, may make S. microcephalus vulnerable to increased fishing pressure in a warming Arctic environment.     

Direct and indirect fishery effects on small coastal elasmobranchs in the northern Gulf of Mexico

Globally, bycatch in tropical/subtropical shrimp trawl and longline fisheries is threatening many marine species. Here we examine the joint effects of increased mortality caused by shrimp trawling bycatch, and reduced predation caused by losses of large sharks because of longline fishing. Research surveys in the Gulf of Mexico (1972–2002) demonstrated precipitous declines in shallow water coastal elasmobranchs where shrimping effort was highest (bonnethead 96%, Bancroft's numbfish (lesser electric ray) 98%, smooth butterfly ray > 99%) and consistent increases in deeper water elasmobranchs (Atlantic angel shark, smooth dogfish). These increases are the first empirical support for predation release caused by the loss of large sharks, which have been theorized to structure tropical/subtropical marine ecosystems. Bycatch of elasmobranchs in shrimp trawls is a critical conservation concern which is not solved by present mitigation measures; similar loss of elasmobranchs is expected to be occurring in tropical/subtropical regions worldwide where ever intensive shrimp trawling occurs.