Asymmetric competition via induced resistance: specialist herbivores indirectly suppress generalist preference and populations

Species may compete indirectly by altering the traits of a shared resource. For example, herbivore-induced responses in plants may make plants more resistant or susceptible to additional herbivorous insect species. Herbivore-induced plant responses can significantly affect interspecific competition and herbivore population dynamics. These herbivore-herbivore indirect interactions have been overlooked in aquatic ecosystems where previous studies used the same herbivore species to induce changes and to assess the effects of these changes. We asked whether seaweed grazing by one of two herbivorous, congeneric snail species (Littorina obtusata or Littorina littorea) with different feeding strategies and preferences would affect subsequent feeding preferences of three herbivore species (both snails and the isopod Idotea baltica) and population densities of three herbivore species (both snails and a third periwinkle snail, Lacuna vincta). In addition, we measured phlorotannin concentrations to test the hypothesis that these metabolites function as induced defenses in the Phaeophyceae. Snail herbivory induced cue-specific responses in apical tissues of the seaweed Fucus vesiculosus that affected the three herbivore species similarly. When compared to ungrazed controls, direct grazing by Littorina obtusata reduced seaweed palatability by at least 52% for both snail species and the isopod species. In contrast, direct grazing by L. littorea did not decrease seaweed palatability for any herbivore, indicating herbivore-specific responses. Previous grazing by L. obtusata reduced populations of L. littorea on outplanted seaweeds by 46% but had no effect on L. obtusata populations. Phlorotannins, a potential class of inducible chemicals in brown algae, were not more concentrated in grazed seaweed tissues, suggesting that some other trait was responsible for the induced resistance. Our results indicate that marine herbivores may compete via inducible responses in shared seaweeds. These plant-mediated interactions were asymmetric with a specialist (L. obtusata) competitively superior to a generalist (L. littorea).     

When there is no escape: the effects of natural enemies on native, invasive, and noninvasive plants

An important question in the study of biological invasions is the degree to which successful invasion can be explained by release from control by natural enemies. Natural enemies dominate explanations of two alternate phenomena: that most introduced plants fail to establish viable populations (biotic resistance hypothesis) and that some introduced plants become noxious invaders (natural enemies hypothesis). We used a suite of 18 phylogenetically related native and nonnative clovers (Trifolium and Medicago) and the foliar pathogens and invertebrate herbivores that attack them to answer two questions. Do native species suffer greater attack by natural enemies relative to introduced species at the same site? Are some introduced species excluded from native plant communities because they are susceptible to local natural enemies? We address these questions using three lines of evidence: (1) the frequency of attack and composition of fungal pathogens and herbivores for each clover species in four years of common garden experiments, as well as susceptibility to inoculation with a common pathogen; (2) the degree of leaf damage suffered by each species in common garden experiments; and (3) fitness effects estimated using correlative approaches and pathogen removal experiments. Introduced species showed no evidence of escape from pathogens, being equivalent to native species as a group in terms of infection levels, susceptibility, disease prevalence, disease severity (with more severe damage on introduced species in one year), the influence of disease on mortality, and the effect of fungicide treatment on mortality and biomass. In contrast, invertebrate herbivores caused more damage on native species in two years, although the influence of herbivore attack on mortality did not differ between native and introduced species. Within introduced species, the predictions of the biotic resistance hypothesis were not supported: the most invasive species showed greater infection, greater prevalence and severity of disease, greater prevalence of herbivory, and greater effects of fungicide on biomass and were indistinguishable from noninvasive introduced species in all other respects. Therefore, although herbivores preferred native over introduced species, escape from pest pressure cannot be used to explain why some introduced clovers are common invaders in coastal prairie while others are not.     

Invasion through quantitative effects: intense shade drives native decline and invasive success.

The effects of invasive nonnative species on community composition are well documented. However, few studies have determined the mechanisms by which invaders drive these changes. The literature indicates that many nonnative plant species alter light availability differently than natives in a given community, suggesting that shading may be such a mechanism. We compared light quantity (photosynthetically active radiation, PAR) and quality (red: far-red ratio, R:Fr) in riparian reaches heavily invaded by a nonnative tree (Acer platanoides) to that in an uninvaded forest and experimentally tested the effects of our measured differences in PAR and R:Fr on the survival, growth, and biomass allocation of seedlings of the dominant native species and Acer platanoides. Light conditions representative of the understory of Acer platanoides-invaded forest decreased survival of the native maple Acer glabrum by 28%; Amelanchier alnifolia by 32%; Betula occidentalis by 55%; Elymus glaucus by 46%; and Sorbus aucuparia by 52%, relative to seedlings growing in PAR similar to that of native understories. In contrast, Acer platanoides and the native shrub Symphoricarpos albus were not affected by reductions in PAR. Acer platanoides seedlings and saplings are uniquely adapted to shade relative to native species. Acer platanoides was the only species tested that decreased allocation to roots relative to shoots in the invaded forest vs. the native forest light conditions. Therefore it was the only species to demonstrate an adaptive response to the particular light environment associated with Acer platanoides invasion as predicted by optimal partitioning theory. The profound change in light quantity associated with Acer platanoides canopies appears to act as an important driver of native suppression and conspecific success in invaded riparian communities. Further research is necessary to determine whether the effect of nonnative plant-driven changes on light quantity and quality is a widespread mechanism negatively affecting resident species and facilitating invasion by nonnatives.     

Comparative water use of native and invasive plants at multiple scales: a global meta-analysis

Ecohydrology and invasive ecology have become increasingly important in the context of global climate change. This study presents the first in-depth analysis of the water use of invasive and native plants of the same growth form at multiple scales: leaf, plant, and ecosystem. We reanalyzed data for several hundred native and invasive species from over 40 published studies worldwide to glean global trends and to highlight how patterns vary depending on both scale and climate. We analyzed all pairwise combinations of co-occurring native and invasive species for higher comparative resolution of the likelihood of an invasive species using more water than a native species and tested for significance using bootstrap methods. At each scale, we found several-fold differences in water use between specific paired invasive and native species. At the leaf scale, we found a strong tendency for invasive species to have greater stomatal conductance than native species. At the plant scale, however, natives and invasives were equally likely to have the higher sap flow rates. Available data were much fewer for the ecosystem scale; nevertheless, we found that invasive-dominated ecosystems were more likely to have higher sap flow rates per unit ground area than native-dominated ecosystems. Ecosystem-scale evapotranspiration, on the other hand, was equally likely to be greater for systems dominated by invasive and native species of the same growth form. The inherent disconnects in the determination of water use when changing scales from leaf to plant to ecosystem reveal hypotheses for future studies and a critical need for more ecosystem-scale water use measurements in invasive- vs. native-dominated systems. The differences in water use of native and invasive species also depended strongly on climate, with the greater water use of invasives enhanced in hotter, wetter climates at the coarser scales.     

The introduction of Littorina littorea to British Columbia, Canada: potential impacts and the importance of biotic resistance by native predators

Although the establishment and spread of non-indigenous species depends upon survival in the face of novel environmental conditions and novel biological interactions, relatively little attention has been focused on the specific role of native predators in limiting invasion success. The European common periwinkle, Littorina littorea, was recently introduced to the Pacific coast of Canada and provides a case study of an introduction into an area with an important predator guild (sea stars) that is functionally minor in the invader’s native habitat. Here, we assess the likelihood of establishment, spread, and negative ecological impact of this introduced gastropod, with an emphasis on the role of native sea stars as agents of biotic resistance. Size frequency distributions and local market availability suggest that L. littorea was most likely introduced via the live seafood trade. Non-native hitchhikers (e.g., the trematode Cryptocotyle lingua) were found on/in both market and field specimens. Laboratory studies and field observations confirmed that L. littorea can survive seasonal low salinity in Vancouver, British Columbia. Periwinkles also readily consumed native Ulva, suggesting that periwinkles could impact native communities via herbivory or resource competition. Unlike native gastropods, however, L. littorea lacked behavioural avoidance responses to Northeast Pacific predatory sea stars (Pisaster ochraceus and Pycnopodia helianthoides), and sea star predation rates on L. littorea were much higher than predation rates on native turban snails (Chlorostoma funebralis) in common garden experiments. We therefore expect periwinkle establishment in British Columbia to be limited to areas with low predator density, as is seen in its field distribution to date. We caution that this conclusion may understate the importance of the L. littorea introduction if it also serves as a vector for additional non-indigenous species such as C. lingua.     

Population and leaf-level variation of iridoid glycosides in the invasive weed Verbascum thapsus L. (common mullein): implications for herbivory by generalist insects

Plant–insect interactions, which are strongly mediated by chemical defenses, have the potential to shape invasion dynamics. Despite this, few studies have quantified natural variation in key defensive compounds of invasive plant populations, or how those defenses relate to levels of herbivory. Here, we evaluated variation in the iridoid glycosides aucubin and catalpol in rosette plants of naturally occurring, introduced populations of the North American invader, Verbascum thapsus L. (common mullein; Scrophulariaceae). We examined two scales that are likely to structure interactions with insect herbivores—among populations and within plant tissues (i.e., between young and old leaves). We additionally estimated the severity of damage incurred at these scales due to insect chewing herbivores (predominantly grasshoppers and caterpillars), and evaluated the relationship between iridoid glycoside content and leaf damage. We found significant variation in iridoid glycoside concentrations among populations and between young and old leaves, with levels of herbivory strongly tracking leaf-level investment in defense. Specifically, across populations, young leaves were highly defended by iridoids (averaging 6.5× the concentration present in old leaves, and containing higher proportions of the potentially more toxic iridoid, catalpol) and suffered only minimal damage from generalist herbivores. In contrast, old leaves were significantly less defended and accordingly more substantially utilized. These findings reveal that quantitative variation in iridoid glycosides is a key feature explaining patterns of herbivory in an introduced plant. In particular, these data support the hypothesis that defenses limit the ability of generalists to feed on mullein’s well-defended young leaves, resulting in minimal losses of high-quality tissue, and increasing performance of this introduced species.     

Eradication via destratification: whole-lake mixing to selectively remove rainbow smelt, a cold-water invasive species

Invasive species can have severe effects on aquatic ecosystems. After invasions occur, eradication should be considered whenever the potential loss of ecosystem services outweighs the cost of the eradication method. Here we evaluate the possibility of destratifying Crystal Lake, Wisconsin, USA, to eradicate the invasive fish rainbow smelt (Osmerus mordax). We modeled the effects of three destratification scenarios (non-, low-, and high-mixing) using both physical and biological models. Field observations were used to calibrate the models. Water temperatures estimated from 18 unique DYRESM simulations were used in a bioenergetics model to estimate growth of five age classes of rainbow smelt under normal and destratified conditions. Our simulations indicate that destratification can eliminate optimal rainbow smelt thermal habitat resulting in mortality. Destratified lake temperatures also surpassed several physiological critical temperatures. Bioenergetics simulations predicted a weight loss of 45-55% in yearling and adult rainbow smelt. We found that destratification is potentially effective for eradicating cold-water species in temperate lakes.     

Female resistance and male preference in a stream-dwelling isopod: effects of female molt characteristics

In the stream-dwelling isopod, Lirceus fontinalis, mating contests between males and females occur prior to pair formation. We examined the relative contribution of male preference and female resistance to contest outcomes. We first quantified male and female behavior during typical mating interactions and examined the relationship between time until molt (TTM) and mating outcomes. We then examined the role of male preference and female resistance in determining mating outcomes when females differed in molt type (growth, egg deposition) and appeared to differ in TTM (due to hormone applications). Both male preference and female resistance contributed to different components of the mating sequence but female resistance ultimately determined whether or not pair formation occurred. Males expressed a preference for females that appeared to be close to molt, using variation in levels of molt hormone as a cue. However, males did not discriminate between females based on molt type. Received: 5 March 1999 / Received in revised form: 10 August 1999 / Accepted: 16 October 1999     

Climatic and Biotic Stochasticity: Disparate Causes of Convergent Demographies in Rare, Sympatric Plants

Abstract:  Species with known demographies may be used as proxies, or approximate models, to predict vital rates and ecological properties of target species that either have not been studied or are species for which data may be difficult to obtain. These extrapolations assume that model and target species with similar properties respond in the same ways to the same ecological factors, that they have similar population dynamics, and that the similarity of vital rates reflects analogous responses to the same factors. I used two rare, sympatric annual plants (sand gilia [ Gilia tenuiflora arenaria ] and Monterey spineflower [ Chorizanthe pungens pungens ]) to test these assumptions experimentally. The vital rates of these species are similar and strongly correlated with rainfall, and I added water and/or prevented herbivore access to experimental plots. Their survival and reproduction were driven by different, largely stochastic factors and processes: sand gilia by herbivory and Monterey spineflower by rainfall. Because the causal agents and processes generating similar demographic patterns were species specific, these results demonstrate, both theoretically and empirically, that it is critical to identify the ecological processes generating observed effects and that experimental manipulations are usually needed to determine causal mechanisms. Without such evidence to identify mechanisms, extrapolations among species may lead to counterproductive management and conservation practices.     

Feeding,food preference,and the uptake of food energy by the supralittoral isopod Ligia pallasii

Analyses of gut contents of freshly collected Ligia pallasii (Brandt) showed that the principal foods were encrusting diatoms, insect larvae, occasional members of the same species, and a variety of red and green seaweeds growing in the upper interiidal tidepool habitat. L. pallasii prefers to eat the green seaweed Ulva sp., and the brown alga Nereocystis luetkeana, when given a choice between several seaweeds, although neither of these forms is normally accessible to the isopods. The absorption (assimilation) of food-energy was 78% on a diet of Ulva and 55 to 76% on a diet of N. luetkeana—representative values for an algivorous invertebrate. A correlation analysis on the relationship of feeding preference of L. pallasii with calorific value of 7 potential seaweed foods suggested that feeding preference in this species is related to factors other than energy content of the food. Food preferences of invertebrates are discussed in relation to calorific value, accessibility, and to various nutritional factors.     

Habitat utilization and alteration by the invasive burrowing isopod, Sphaeroma quoyanum, in California salt marshes

In recent years the pace of exotic species introduction and invasion has accelerated, particularly in estuaries and wetlands. Species invasions may affect coastal ecosystems in many ways. Alteration of sedimentary environments, through structure formation and burrowing, has particularly dramatic effects on coastal habitats. This study examines modification of channel bank and marsh edge habitat by the burrowing Australasian isopod Sphaeroma quoyanum Milne Edwards, in created and natural salt marshes of San Diego Bay and San Francisco Bay. Abundance and distribution patterns of this isopod species, its relationships with habitat characteristics, and its effects on sediment properties and bank erosion were examined seasonally, and in several marsh microhabitats. Mean isopod densities were 1541 and 2936 individuals per 0.25 m² in San Francisco Bay, and 361 and 1153 individuals per 0.25 m² in San Diego Bay study sites during December and July 1998, respectively. This isopod forms dense, anastomosing burrow networks. S. quoyanum densities did not differ as a function of location within creeks or location in natural versus created marshes. Burrows, which are on average 6 mm wide and 2 cm long, were associated with firm sediments containing high detrital biomass. Although erosion is a natural process along salt marsh banks, enclosure experiments demonstrated that isopod activities can enhance sediment loss from banks. In areas infested with S. quoyanum, losses may exceed 100 cm of marsh edge per year. The effects of habitat alteration by this invading species are likely to increase in severity in the coastal zone as these ecosystems become degraded. Received: 30 March 2000 / Accepted: 21 September 2000     

Population regulation by enemies of the grass Brachypodium sylvaticum: demography in native and invaded ranges

The enemy-release hypothesis (ERH) states that species become more successful in their introduced range than in their native range because they leave behind natural enemies in their native range and are thus "released" from enemy pressures in their introduced range. The ERH is popularly cited to explain the invasive properties of many species and is the underpinning of biological control. We tested the prediction that plant populations are more strongly regulated by natural enemies (herbivores and pathogens) in their native range than in their introduced range with enemy-removal experiments using pesticides. These experiments were replicated at multiple sites in both the native and invaded ranges of the grass Brachypodium sylvaticum. In support of the ERH, enemies consistently regulated populations in the native range. There were more tillers and more seeds produced in treated vs. untreated plots in the native range, and few seedlings survived in the native range. Contrary to the ERH, total measured leaf damage was similar in both ranges, though the enemies that caused it differed. There was more damage by generalist mollusks and pathogens in the native range, and more damage by generalist insect herbivores in the invaded range. Demographic analysis showed that population growth rates were lower in the native range than in the invaded range, and that sexually produced seedlings constituted a smaller fraction of the total in the native range. Our removal experiment showed that enemies regulate plant populations in their native range and suggest that generalist enemies, not just specialists, are important for population regulation.     

Effects of vegetation cover, presence of a native ant species, and human disturbance on colonization by Argentine ants

The spread of non-native invasive species is affected by human activity, vegetation cover, weather, and interaction with native species. We analyzed data from a 17-year study of the distribution of the non-native Argentine ant (Linepithema humile) and the native winter ant (Prenolepis imparis) in a preserve in northern California (U.S.A.). We conducted logistic regressions and used model selection to determine whether the following variables were associated with changes in the distribution of each species: presence of conspecifics at neighboring sites, distance to development (e.g., roads, buildings, and landscaped areas), proportion of vegetation cover taller than 0.75 m, elevation, distance to water, presence of both species at a site, temperature, and rainfall. Argentine ants colonized unoccupied sites from neighboring sites, but the probability of appearance and persistence decreased as distance to development, vegetation cover, and elevation increased. Winter ants appeared and persisted in sites with relatively high vegetation cover (i.e., highly shaded sites). Presence of the 2 species was negatively associated in sites with high vegetation cover (more winter ants) and sites near development (more Argentine ants). Probability of colonization of Argentine ants decreased where winter ants were most persistent. At sites near development within the preserve, abundant Argentine ant populations may be excluding winter ants. The high abundance of Argentine ants at these sites may be due to immigration from suburban areas outside the preserve, which are high-quality habitat for Argentine ants. In the interior of the preserve, distance from development, low-quality habitat, and interaction with winter ants may in combination exclude Argentine ants. Interactions among the variables we examined were associated with low probabilities of Argentine ant colonization in the preserve.     

Prey defense,predator preference,and nonrandom diet: The interactions between Pycnopodia helianthoides and two species of sea urchins

Interactions between the predatory sea star Pycnopodia helianthoides (Brandt, 1835) and two of its natural prey, the sea urchins Strongylocentrotus purpuratus (Stimpson, 1857) and S. franciscanus (Agassiz, 1863), are examined with regard to predator preference, predator diet, and prey defenses. The sea star is able to detect both species of sea urchin upstream in a Y-trough, but does not consistently choose one over the other (i.e., no preference). However, when the sea star is presented with equal numbers of similar-sized specimens of the two species of sea urchin, its diet is markedly nonrandom, since S. purpuratus is eaten almost 98% of the time. The defensive responses of the two species of sea urchin differ in form and effectiveness. S. franciscanus employs its long spines as defensive weapons, pinching the rays of an attacking sea star. This defensive response is more effective than the pedicellarial response used by S. purpuratus. The nonrandom diet of the predator seems to result primarily from prey defensive responses that differ in effectiveness, rather than from an intrinsic, behavioral preference of the predator at an earlier stage in the predator/prey interaction.     

Host preference,site fidelity,and homing behavior of the symbiotically luminous cardinalfish,Siphamia tubifer (Perciformes: Apogonidae)

The sea urchin cardinalfish, Siphamia tubifer (Perciformes: Apogonidae), is unusual among coral reef fishes for its use of bioluminescence, produced by symbiotic bacteria, while foraging at night. As a foundation for understanding the relationship between the symbiosis and the ecology of the fish, this study examined the diel behavior, host urchin preference, site fidelity, and homing of S. tubifer in June and July of 2012 and 2013 at reefs near Sesoko Island, Okinawa, Japan (26°38′N, 127°52′E). After foraging, S. tubifer aggregated in groups among the spines of the longspine sea urchin, Diadema setosum, and the banded sea urchin, Echinothrix calamaris. A preference for D. setosum was evident (P < 0.001), especially by larger individuals (>25 mm standard length, P < 0.01), and choice experiments demonstrated the ability of S. tubifer to recognize and orient to a host urchin and to conspecifics. Tagging studies revealed that S. tubifer exhibits daily fidelity to a host urchin; 43–50 and 26–37 % of tagged individuals were associated with the same urchin after 3 and 7 days. Tagged fish also returned to their site of origin after displacement; by day two, 23–43 and 27–33 % of tagged individuals returned from displacement distances of 1 and 2 km. These results suggest that S. tubifer uses various environmental cues for homing and site fidelity; similar behaviors and cues might be used by larvae for recruitment to settlement sites and for the acquisition of luminous symbiotic bacteria.     

Differences between native and invasive<Emphasis Type="Italic"> Caulerpa taxifolia</Emphasis>: a link between asexual fragmentation and abundance in invasive populations

The tropical and subtropical marine green alga Caulerpa taxifolia has invaded several temperate regions throughout the world, including southeastern Australia. In this study, I examined how invasive C. taxifolia from temperate southeastern Australia differed from native C. taxifolia from subtropical Moreton Bay, Australia, in the traits proposed as being important to its invasion success: thallus size and density, levels of asexual reproduction (fragmentation) and total biomass. Against the prediction of a large size for invasive C. taxifolia, native populations from Moreton Bay had larger stolons and fronds than invasive populations. However, invasive populations consistently had much higher densities of stolons, fronds and fragmented fronds; and a greater biomass compared to native populations. Average densities at invasive sites exceeded 4,700 stolons and 9,000 fronds/m² and were as high as 27,000 stolons and 95,000 fronds/m², which are the highest reported for C. taxifolia anywhere. Average densities of fragmented fronds at invasive sites were as high as 6,000/m² and up to 45% of all stolons at invasive sites could be directly linked to asexual recruitment via fragmented fronds. Importantly, at invasive locations there was a strong association between asexual reproduction and abundance demonstrated by positive correlations between the density of fragmented fronds and total biomass. These findings are the first to describe quantitative differences between native and invasive C. taxifolia and to demonstrate a link between the high levels of asexual reproduction and high abundance in invasive populations. Although the causes and consequences of high levels of asexual reproduction remain to be explored, this study suggests that changes in demographic and life-history traits during the invasion by C. taxifolia into temperate habitats may contribute to its success there.Communicated by M. S. Johnson, Crawley     

Antipredator responses to invasive lionfish, Pterois volitans: interspecific differences in cue utilization by two coral reef gobies

Understanding prey response to predators and their utilization of sensory cues to assess local predation risk is crucial in determining how predator avoidance strategies affect population demographics. This study examined the antipredator behaviors of two ecologically similar species of Caribbean coral reef fish, Coryphopterus glaucofraenum and Gnatholepis thompsoni, and characterized their responses to different reef predators. In laboratory assays, the two species of gobies were exposed to predator visual cues (native Nassau grouper predator vs. invasive lionfish predator), damage-released chemical cues from gobies, and combinations of these, along with appropriate controls. Behavioral responses indicate that the two prey species differ in their utilization of visual and chemical cues. Visual cues from predators were decisive for both species’ responses, demonstrating their relative importance in the sensory hierarchy, whereas damage-released cues were a source of information only for C. glaucofraenum. Both prey species could distinguish between native and invasive predators and subsequently altered their antipredator responses.