Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions

We present a framework for explaining variation in predator invasion success and predator impacts on native prey that integrates information about predator–prey naïveté, predator and prey behavioral responses to each other, consumptive and non-consumptive effects of predators on prey, and interacting effects of multiple species interactions. We begin with the ‘naïve prey’ hypothesis that posits that naïve, native prey that lack evolutionary history with non-native predators suffer heavy predation because they exhibit ineffective antipredator responses to novel predators. Not all naïve prey, however, show ineffective antipredator responses to novel predators. To explain variation in prey response to novel predators, we focus on the interaction between prey use of general versus specific cues and responses, and the functional similarity of non-native and native predators. Effective antipredator responses reduce predation rates (reduce consumptive effects of predators, CEs), but often also carry costs that result in non-consumptive effects (NCEs) of predators. We contrast expected CEs versus NCEs for non-native versus native predators, and discuss how differences in the relative magnitudes of CEs and NCEs might influence invasion dynamics. Going beyond the effects of naïve prey, we discuss how the ‘naïve prey’, ‘enemy release’ and ‘evolution of increased competitive ability’ (EICA) hypotheses are inter-related, and how the importance of all three might be mediated by prey and predator naïveté. These ideas hinge on the notion that non-native predators enjoy a ‘novelty advantage’ associated with the naïveté of native prey and top predators. However, non-native predators could instead suffer from a novelty disadvantage because they are also naïve to their new prey and potential predators. We hypothesize that patterns of community similarity and evolution might explain the variation in novelty advantage that can underlie variation in invasion outcomes. Finally, we discuss management implications of our framework, including suggestions for managing invasive predators, predator reintroductions and biological control.

Indirect and direct controls of macroinvertebrates and small fish by abiotic factors and trophic interactions in the Florida Everglades

1. The roles of nutrients, disturbance and predation in regulating consumer densities have long been of interest, but their indirect effects have rarely been quantified in wetland ecosystems. The Florida Everglades contains gradients of hydrological disturbance (marsh drying) and nutrient enrichment (phosphorus), often correlated with densities of macroinvertebrate infauna (macroinvertebrates inhabiting periphyton), small fish and larger invertebrates, such as snails, grass shrimp, insects and crayfish. However, most causal relationships have yet to be quantified. 2.  We sampled periphyton (content and community structure) and consumer (small omnivores, carnivores and herbivores, and infaunal macroinvertebrates inhabiting periphyton) density at 28 sites spanning a range of hydrological and nutrient conditions and compared our data to seven a priori structural equation models. 3.  The best model included bottom-up and top-down effects among trophic groups and supported top-down control of infauna by omnivores and predators that cascaded to periphyton biomass. The next best model included bottom-up paths only and allowed direct effects of periphyton on omnivore density. Both models suggested a positive relationship between small herbivores and small omnivores, indicating that predation was unable to limit herbivore numbers. Total effects of time following flooding were negative for all three consumer groups even when both preferred models suggested positive direct effects for some groups. Total effects of nutrient levels (phosphorus) were positive for consumers and generally larger than those of hydrological disturbance and were mediated by changes in periphyton content. 4.  Our findings provide quantitative support for indirect effects of nutrient enrichment on consumers, and the importance of both algal community structure and periphyton biomass to Everglades food webs. Evidence for top-down control of infauna by omnivores was noted, though without substantially greater support than a competing bottom-up-only model.

Top down control in a relatively pristine seagrass ecosystem

The loss of large-bodied herbivores and/or top predators has been associated with large-scale changes in terrestrial, freshwater, and marine ecosystems around the world. Understanding the consequences of these declines has been hampered by a lack of studies in relatively pristine systems. To fill this gap, I investigated the dynamics of the relatively pristine seagrass ecosystem of Shark Bay, Australia. I began by examining the seagrass species distributions, stoichiometry, and patterns of nutrient limitation across the whole of Shark Bay. Large areas were N-limited, P-limited, or limited by factors other than nutrients. Phosphorus-limitation was centered in areas of restricted water exchange with the ocean. Nutrient content of seagrasses varied seasonally, but the strength of seasonal responses were species-specific. Using a cafeteria-style experiment, I found that fast-growing seagrass species, which had higher nutrient content experienced higher rates of herbivory than slow-growing species that are dominant in the bay but have low nutrient content. Although removal rates correlated well with nutrient content at a broad scale, within fast-growing species removal rates were not closely tied to N or P content. Using a combination of stable isotope analysis and animal borne video, I found that green turtles (Chelonia mydas)—one of the most abundant large-bodied herbivores in Shark Bay—appear to assimilate little energy from seagrasses at the population level. There was, however, evidence of individual specialization in turtle diets with some individuals foraging largely on seagrasses and others feeding primarily on macroalgae and gelatinous macroplankton. Finally, I used exclusion cages, to examine whether predation-sensitive habitat shifts by megagrazers (green turtles, dugongs) transmitted a behavior-mediated trophic cascade (BMTC) between sharks and seagrasses. In general, data were consistent with predictions of a behavior-mediated trophic cascade. Megaherbivore impacts on seagrasses were large only in the microhabitat where megaherbivores congregate to reduce predation risk. My study highlights the importance of large herbivores in structuring seagrass communities and, more generally, suggests that roving top predators likely are important in structuring communities—and possibly ecosystems—through non-consumptive pathways.

Population viability analyses of Chamaecrista keyensis (Leguminosae: Caesalpinioideae), a narrowly endemic herb of the lower Florida Keys: Effects of seasonal timing of fires and the urban -wildland interface

This research first evaluated the effects of urban wildland interface on reproductive biology of the Big Pine Partridge Pea, Chamaecrista keyensis, an understory herb that is endemic to Big Pine Key, Florida. I found that C. keyensis was self-compatible, but depended on bees for seed set. Furthermore, individuals of C. keyensis in urban habitats suffered higher seed predation and therefore set fewer seeds than forest interior plants. ^ I then focused on the effects of fire at different times of the year, summer (wet) and winter (dry), on the population dynamics and population viability of C. keyensis. I found that C. keyensis population recovered faster after winter burns and early summer burns (May–June) than after late summer burns (July–September) due to better survival and seedling recruitment following former fires. Fire intensity had positive effects on reproduction of C. keyensis. In contrast, no significant fire intensity effects were found on survival, growth, and seedling recruitment. This indicated that better survival and seedling recruitment following winter and early summer burns (compared with late summer burns) were due to the reproductive phenology of the plant in relation to fires rather than differences in fire intensity. Deterministic population modeling showed that time since fire significantly affected the finite population growth rates (λ). Particularly, recently burned plots had the largest λ. In addition, effects of timing of fires on λ were most pronounced the year of burn, but not the subsequent years. The elasticity analyses suggested that maximizing survival is an effective way to minimize the reduction in finite population growth rate the year of burn. Early summer fires or dry-season fires may achieve this objective. Finally, stochastic simulations indicated that the C. keyensis population had lower extinction risk and population decline probability if burned in the winter than in the late summer. A fire frequency of approximately 7 years would create the lowest extinction probability for C. keyensis. A fire management regime including a wide range of burning seasons may be essential for the continued existence of C. keyensis and other endemic species of pine rockland on Big Pine Key. ^

Fish Community Responses to the Combined Effects of Decreased Hydroperiod and Nonnative Fish Invasions in a Karst Wetland: Are Everglades Solution Holes Sinks for Native Fishes?

Short-hydroperiod Everglades wetlands have been disproportionately affected by reductions in freshwater inflows, land conversion and biotic invasions. Severe hydroperiod reductions in these habitats, including the Rocky Glades, coupled with proximity to canals that act as sources of invasions, may limit their ability to support high levels of aquatic production. We examined whether karst solution holes function as dry-down refuges for fishes, providing a source of marsh colonists upon reflooding, by tracking fish abundance, nonnative composition, and survival in solution holes throughout the dry season. We paired field surveys with an in situ nonnative predation experiment that tested the effects of predation by the recent invader, African jewelfish (Hemichromis letourneuxi) on native fishes. Over the 3 years surveyed, a large number of the solution holes dried before the onset of the wet season, while those retaining water had low survivorship and were dominated by nonnatives. In the experiment, mortality of eastern mosquitofish (Gambusia holbrooki) in the presence of African jewelfish was greater than that associated with deteriorating water quality. Under current water management, findings suggest that solution holes are largely sinks for native fishes, given the high frequency of drydown, extensive period of fish residence, and predation by nonnative fishes.

Contrasting patterns of individual specialization and trophic coupling in two marine apex predators

1. Apex predators are often assumed to be dietary generalists and, by feeding on prey from multiple basal nutrient sources, serve to couple discrete food webs. But there is increasing evidence that individual level dietary specialization may be common in many species, and this has not been investigated for many marine apex predators. 2. Because of their position at or near the top of many marine food webs, and the possibility that they can affect populations of their prey and induce trophic cascades, it is important to understand patterns of dietary specialization in shark populations. 3. Stable isotope values from body tissues with different turnover rates were used to quantify patterns of individual specialization in two species of ‘generalist’ sharks (bull sharks, Carcharhinus leucas, and tiger sharks, Galeocerdo cuvier). 4. Despite wide population-level isotopic niche breadths in both species, isotopic values of individual tiger sharks varied across tissues with different turnover rates. The population niche breadth was explained mostly by variation within individuals suggesting tiger sharks are true generalists. In contrast, isotope values of individual bull sharks were stable through time and their wide population level niche breadth was explained by variation among specialist individuals. 5. Relative resource abundance and spatial variation in food-predation risk tradeoffs may explain the differences in patterns of specialization between shark species. 6. The differences in individual dietary specialization between tiger sharks and bull sharks results in different functional roles in coupling or compartmentalizing distinct food webs. 7. Individual specialization may be an important feature of trophic dynamics of highly mobile marine top predators and should be explicitly considered in studies of marine food webs and the ecological role of top predators.

A Suite of Prey Traits Determine Predator and Nutrient Enrichment Effects in a Tri-Trophic Food Chain

Predation, predation risk, and resource quality affect suites of prey traits that collectively impact individual fitness, population dynamics, and community structure. However, studies of multi-trophic level effects generally focus on a single prey trait, failing to capture trade-offs among suites of covarying traits that govern population responses and emergent community patterns. We used structural equation models (SEM) to summarize the non-lethal and lethal effects of crayfish, Procambarus fallax, and phosphorus (P) addition, which affected prey food quality (periphyton), on the interactive effects of behavioral, morphological, developmental, and reproductive traits of snails, Planorbella duryi. Univariate and multivariate analyses suggested trade-offs between production (growth, reproduction) and defense (foraging behavior, shell shape) traits of snails in response to non-lethal crayfish and P addition, but few lethal effects. SEM revealed that non-lethal crayfish effects indirectly limited per capita offspring standing stock by increasing refuge use, slowing individual growth, and inducing snails to produce thicker, compressed shells. The negative effects of non-lethal crayfish on snails were strongest with P addition; snails increased allocation to shell defense rather than growth or reproduction. However, compared to ambient conditions, P addition with non-lethal crayfish still yielded greater per capita offspring standing stock by speeding individual snail growth enabling them to produce more offspring that also grew faster. Increased refuge use in response to non-lethal crayfish led to a non-lethal trophic cascade that altered the spatial distribution of periphyton. Independent of crayfish effects, snails stimulated periphyton growth through nutrient regeneration. These findings illustrate the importance of studying suites of traits that reveal costs associated with inducing different traits and how expressing those traits impacts population and community level processes.

Using stable isotopes to investigate trophic interactions of bottlenose dolphins (Tursiops truncatus) in the Florida Coastal Everglades

Top predators are known for their ability to 1) affect their communities through predation and 2) induce behavioral modifications. Recent research suggests that they may also play “bottom-up” roles in ecosystems, including transporting materials within and across habitat boundaries. The Florida Coastal Everglades (FCE) is an “upside-down” oligotrophic estuary where productivity decreases from the mouth of the estuary to freshwater marshes. Therefore, movements of predators may be important in ecosystem dynamics. While other estuarine predators in the FCE have been shown to potentially move nutrients among ecosystems, the potential for bottlenose dolphins (Tursiops truncatus) to play a similar role in the systems has not been investigated. Stable isotope analysis of biopsy samples were used to investigate spatial variation in trophic interactions of dolphins to see if they might transport nutrients. Values of δ15 N suggest dolphins feed at a trophic level similar to other top predators in the ecosystem while δ13 C suggest that dolphins forage largely within food webs where they were sampled rather than transporting nutrients across ecosystem boundaries. The exception may be dolphins foraging in rivers, which may transport nutrients downstream; a pattern opposite to that of bull sharks and alligators in these habitats. Further research is necessary to predict how future changes occurring due to restoration and climate will affect the ecological roles of dolphins.

Understanding the role of Dimethylsulfoniopropionate as a potential chemotactic cue for coral-associated bacteria

Most reef-building corals are known to engage in non-pathogenic symbiosis not only with unicellular dinoflagellates from the genus Symbiodinium, but also with other microscopic organisms such as bacteria, fungi, and viruses. The functional details of these highly complex associations remain largely unclear. The impetus of this study is to gain a better understanding of the symbiotic interaction between marine bacteria and their coral host. Studies have shown that certain bacterial orders associate with specific certain coral species, thus making the symbiotic synergy a non-random consortium. Consequently both corals and bacteria may be capable of emitting chemical cues that enable both parties to find one another and thus generate the symbiosis. The production of these cues by the symbionts may be the result of environmental stimuli such as elevated ocean temperatures, increased water acidity, and even predation. One potential chemical cue could be the compound DMSP (Dimethylsulfoniopropionate) and its sulphur derivatives. Reef-building corals are believed to be the major producers of the DMSP during times of stress. Marine bacteria utilize DMSP as a source of sulfur and carbon. As a result corals could potentially attract their bacterial consortium depending on their DMSP production. This would enable them to adapt to fluctuating environmental conditions by changing their bacterial communities to that which may aid in survival. To test the hypothesis that coral-produced DMSP plays a role in attracting symbiotic bacteria, this study utilized the advent of high-throughput sequencing paired with chemotactic assays to determine the response of coral-associated bacterial isolates towards the DMSP compound at differing concentrations. Chemotaxis assays revealed that some isolates responded positively towards the DMSP compound. This finding adds to existing evidence suggesting that coral-associated pathogens utilize chemotaxis as a host colonization and detection mechanism. Thus the symbiotic bacteria that make up the coral microbiome may also employ this process. Furthermore this study demonstrates that bacterial motility may be a strong contributing factor in the response to the chemotactic cue. Swarming motility may be better suited for bacteria that need to respond to a chemical gradient on the surface of the coral. Therefore the isolates that were able to swarm seemed to respond more strongly to the DMSP.

Understanding anuran community dynamics in temporary wetlands: the interaction and importance of landscape and biotic processes

The major objective of this study was to determine the relative importance of landscape factors, local abiotic factors, and biotic interactions in influencing tadpole community structure in temporary wetlands. I also examined the influence of agricultural activities in South-central Florida by comparing tadpole communities in native prairie wetlands (a relatively unmodified habitat) at the Kissimmee Prairie Sanctuary (KPS) to tadpole communities in three agriculturally modified habitats found at MacArthur Agro- Ecology Research Center (MAERC). Environmental characteristics were measured in 24 isolated wetlands, and tadpoles were sampled using throw-traps and dipnets during the 1999 wet season (June - October). Landscape characteristics were expected to predominately influence all aspects of community structure because anurans associated with temporary wetland systems are likely to exist as metapopulations. Both landscape characteristics (wetland proximity to nearest woodland and the amount of woodland surrounding the wetland) and biotic interactions (fish predation) had the largest influence on tadpole community structure. Predatory fish influenced tadpole communities more than expected due to the ubiquity of wetlands, lack of topographic relief, and dispersal abilities of several fish species. Differences in tadpole community structure among habitat types were attributed to differences in woodland attributes and susceptibility to fish colonization. Furthermore, agricultural modification of prairie habitats in South-central Florida may benefit amphibian communities, particularly woodland-dwelling species that are unable to coexist with predatory fish. From a conservation standpoint, temporary wetlands proximal to woodland areas and isolated from permanent water sources appear to be most important to amphibians. In addition, the high tadpole densities attained in these wetlands suggest that these wetlands serve as biological hotspots within the landscape, and their benefits extend into the adjacent terrestrial matrix. Further research efforts are needed to quantify the biological productivity of these systems and determine spatial dynamics of anurans in surrounding terrestrial habitats.

Non-consumptive effects of predators in coral reef communities and the indirect consequences of marine protected areas

Predators exert strong direct and indirect effects on ecological communities by intimidating their prey. Non-consumptive effects (NCEs) of predators are important features of many ecosystems and have changed the way we understand predator-prey interactions, but are not well understood in some systems. For my dissertation research I combined a variety of approaches to examine the effect of predation risk on herbivore foraging and reproductive behaviors in a coral reef ecosystem. In the first part of my dissertation, I investigated how diet and territoriality of herbivorous fish varied across multiple reefs with different levels of predator biomass in the Florida Keys National Marine Sanctuary. I show that both predator and damselfish abundance impacted diet diversity within populations for two herbivores in different ways. Additionally, reef protection and the associated recovery of large predators appeared to shape the trade-off reef herbivores made between territory size and quality. In the second part of my dissertation, I investigated context-dependent causal linkages between predation risk, herbivore foraging behavior and resource consumption in multiple field experiments. I found that reef complexity, predator hunting mode, light availability and prey hunger influenced prey perception of threat and their willingness to feed. This research argues for more emphasis on the role of predation risk in affecting individual herbivore foraging behavior in order to understand the implications of human-mediated predator removal and recovery in coral reef ecosystems.^

Data compilation on the biological response to ocean acidification: environmental and experimental context of data sets and related literature

The exponential growth of studies on the biological response to ocean acidification over the last few decades has generated a large amount of data. To facilitate data comparison, a data compilation hosted at the data publisher PANGAEA was initiated in 2008 and is updated on a regular basis (doi:10.1594/PANGAEA.149999). By January 2015, a total of 581 data sets (over 4 000 000 data points) from 539 papers had been archived. Here we present the developments of this data compilation five years since its first description by Nisumaa et al. (2010). Most of study sites from which data archived are still in the Northern Hemisphere and the number of archived data from studies from the Southern Hemisphere and polar oceans are still relatively low. Data from 60 studies that investigated the response of a mix of organisms or natural communities were all added after 2010, indicating a welcomed shift from the study of individual organisms to communities and ecosystems. The initial imbalance of considerably more data archived on calcification and primary production than on other processes has improved. There is also a clear tendency towards more data archived from multifactorial studies after 2010. For easier and more effective access to ocean acidification data, the ocean acidification community is strongly encouraged to contribute to the data archiving effort, and help develop standard vocabularies describing the variables and define best practices for archiving ocean acidification data.

Conservação genética da orquídea Cattleya granulosa Lindley

Cattleya granulosa Lind is a large and endemic orchid in Atlantic Forest fragments in Northeast Brazil. The facility of collecting, uniqueness of their flowers, which have varying colors between green and reddish brown, and distribution in coastal areas of economic interest make their populations a constant target of predation, which also suffer from environmental degradation. Due to the impact on their populations, the species is threatened. In this study, we evaluate the levels of spatial aggregation in a preserved population, analyze the phylogenetic relationships of C. granulosa Lindl. with four other Laeliinae species (Brassavola tuberculata, C. bicolor, C. labiata and C. schofieldiana) and also to evaluate the genetic diversity of 12 remaining populations of C. granulosa Lindl. through ISSR. There was specificity of epiphytic C. granula Lindl. with a single host tree, species of Eugenia sp. C. granulosa Lindl. own spatial pattern, with the highest density of neighbors within up to 5 m. Regarding the phylogenetic relationships and genetic patterns with other species of the genus, C. bicolor exhibited the greatest genetic diversity (HE = 0.219), while C. labiata exhibited the lowest level (HE = 0.132). The percentage of genetic variation among species (AMOVA) was 23.26%. The principal component analysis (PCA) of ISSR data showed that unifoliate and bifoliolate species are genetically divergent. PCA indicated a close relationship between C. granulosa Lindl. and C. schofieldiana, a species considered to be a variety of C. granulosa Lindl. by many researchers. Population genetic analysis using ISSR showed all polymorphic loci. The high genetic differentiation between populations (ФST = 0.391, P < 0.0001) determined the structure into nine groups according to log-likelihood of Bayesian analysis, with a similar pattern in the dendrogram (UPGMA) and PCA. A positive and significant correlation between geographic and genetic distances between populations was identified (r = 0.794, P = 0.017), indicating isolation by distance. Patterns of allelic diversity suggest the occurrence of population bottlenecks in most populations of C. granulosa Lindl. (n = 8). Genetic data indicate that enable the maintenance of genetic diversity of the species is complex and is directly related to the conservation of different units or groups that are spatially distant.

Gato-do-mato-pequeno (Leopardus tigrinus) na Caatinga: ocupação e padrão de atividade de um felídeo ameaçado e pouco conhecido na floresta tropical seca do nordeste do Brasil

While the carnivores are considered regulators and structuring of natural communities are also extremely threatened by human activities. Endangered little-spotted-cat (Leopardus tigrinus) is one of the lesser known species from the Neotropical cats. In this work we investigate the occupancy and the activity pattern of L. tigrinus in Caatinga of Rio Grande do Norte testing: 1) how environmental and anthropogenic factors influence their occupation and 2) how biotic and abiotic factors influence their activity pattern. For this we raised occurrence data of species in 10 priority areas for conservation. We built hierarchical models of occupancy based on maximum likelihood to represent biological hypotheses which were ranked using the Akaike Information Criterion (AIC). According to the results the feline occupancy is more likely away from rural settlements and in areas with a higher proportion of woody vegetation. The opportunistic killing of L. tigrinus and in retaliation for poultry predation close to residential areas can explain this result; as well as more complex vegetation structure can better serve as refuge and ensure more food. Analyzing the records of the species through circular statistics we conclude that the activity pattern is mostly nocturnal, although considerable crepuscular and a small diurnal activity. L. tigrinus activity was directly affected by the availability of small terrestrial mammals, which are essentially nocturnal. In addition, the temperatures recorded in the environment directly and indirectly affect the activity of the little-spotted-cat, as also influence the activity of their potential prey. Generally, the cats were more active when possible prey were active, and this happened at night when lower temperatures are recorded. Moreover, the different lunar phases did not affect the activity pattern. The results improve the understanding of an endangered feline inhabiting the Caatinga biome, and thus can help develop conservation and management strategies, as well as in planning future research in this semi-arid ecosystem.

Biologia reprodutiva de Mimus gilvus (Aves: Mimidae) em área de restinga no nordeste do Brasil

The thrush beach, Mimus gilvus (Aves: Mimidae) is a passerine widely distributed in Central and South America. In Brazil occurs mainly in the areas of the resting and vegetation near the beach. In southeastern Brazil this species has disappeared, mainly due to urbanization. Many attributes of their reproductive biology are unknown, especially in relation to reproductive success. During the years 2010-2011, 2011-2012 and 2014-2015 were made visits to the area of restinga forest in Centro de Lançamento da Barreira do Inferno (CLBI), located between the cities of Natal and Parnamirim-RN (5 ° 54'S 35 ° 10'W ) where they were made systematic searches to trying describe reproductive biology of the characteristics of M. gilvus, estimate their reproductive success using the Mayfield method, and identify the main factors that influence their reproductive success in environment the resting. For this, forty fifth active nests monitored were used. Only during the breeding season of 2011-2012 and 2014-2015 were made systematic visits to the study area. The reproductive period ranged August to March. Clutch size ranged from two, three and six eggs (n = 22). Broods of two eggs were more common, with an average of eggs laid per nest of 2 ± 0,51 (n = 20 nests). The incubation period was approximately 13 ± 1,9 days (n = 11 nests). The period of stay of the nestlings was approximately 11 ± 1,6 days (n = 9 nests). With approximately 11 days old the nestlings were able to leave the nest. The apparent success was 37,8% and the success estimated by Mayfield method was 26,6%. Predation was the main cause of loss of nests in the study area. The daily survival rates (TDS) were obtained from 0,9593 incubation and 0,9313 for nestling period respectively. Survival estimates for each period was 0,5827 for incubation and 0,4571 for nestling period. The cumulative average rainfall for each month influenced negatively the hatching rates of M. gilvus nests. In addition, the number hatch eggs among the most rainy season (rainy season) and the period of lowest rainfall (dry season) were different. The number of lost nests of M. gilvus was lower in scrubs than cactus, which may account for the largest number of nests of this species found in scrubs. Survival rates in nestling period were lower compared with the incubation period. The fact that the survival rates nests of M. gilvus be lower in the nestling period compared to the incubation period may result from increased activity of adults during this phase of the nest, which in turn would increase predation rates. M. gilvus seems to avoid the rainy season during their reproduction, concentrated most of their nests in periods of low rainfall.