No abstract

Interspecific interactions play an important role in the success of introduced species. For example, the ‘enemy release’ hypothesis posits that introduced species become invasive because they escape top–down regulation by natural enemies while the ‘invasional meltdown’ hypothesis posits that invasions may be facilitated by synergistic interactions between introduced species. Here, we explore how facilitation and enemy release interact to moderate the potential effect of a large category of positive interactions – protection mutualisms. We use the interactions between an introduced plant (Japanese knotweed Fallopia japonica), an introduced herbivore (Japanese beetle Popillia japonica), an introduced ant (European red ant Myrmica rubra), and native ants and herbivores in riparian zones of the northeastern United States as a model system. Japanese knotweed produces sugary extrafloral nectar that is attractive to ants, and we show that both sugar reward production and ant attendance increase when plants experience a level of leaf damage that is typical in the plants’ native range. Using manipulative experiments at six sites, we demonstrate low levels of ant patrolling, little effect of ants on herbivory rates, and low herbivore pressure during midsummer. Herbivory rates and the capacity of ants to protect plants (as evidenced by effects of ant exclusion) increased significantly when plants were exposed to introduced Japanese beetles that attack plants in the late summer. Beetles were also associated with greater on‐plant foraging by ants, and among‐plant differences in ant‐foraging were correlated with the magnitude of damage inflicted on plants by the beetles. Last, we found that sites occupied by introduced M. rubra ants almost invariably included Japanese knotweed. Thus, underlying variation in the spatiotemporal distribution of the introduced herbivore influences the provision of benefits to the introduced plant and to the introduced ant. More specifically, the presence of the introduced herbivore converts an otherwise weak interaction between two introduced species into a reciprocally beneficial mutualism. Because the prospects for facilitation are linked to the prospects for enemy release in protection mutualisms, species introductions can have complex effects on existing species interactions, between both native and introduced species.

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Predation by nonnative fishes has reduced abundance and increased extinction risk for amphibian populations worldwide. Although rare, fish and palatable amphibians have been observed to coexist where aquatic vegetation and structural complexity provide suitable refugia. We examined whether larval Long-toed Salamanders (Ambystoma macrodactylum Baird, 1850) increased use of vegetation cover in lakes with trout and whether adding vegetation structure could reduce predation risk and nonconsumptive effects (NCEs), such as reductions in body size and delayed metamorphosis. We compared use of vegetation cover by larval salamanders in lakes with and without trout and conducted a field experiment to investigate the influence of added vegetation structure on salamander body morphology and life history. The probability of catching salamanders in traps in lakes with trout was positively correlated with the proportion of submerged vegetation and surface cover. Growth rates of salamanders in enclosures with trout cues decreased as much as 85% and the probability of metamorphosis decreased by 56%. We did not find evidence that adding vegetation reduced NCEs in experimental enclosures, but salamanders in lakes with trout used more highly vegetated areas, which suggests that adding vegetation structure at the scale of the whole lake may facilitate coexistence between salamanders and introduced trout.

No abstract

Translocations are stressful, especially when captive animals are naïve to natural stimuli. Captive eastern hellbenders (Cryptobranchus alleganiensis alleganiensis) identify predatory fish as threats, but may be more vulnerable to predation and stress because of inexperience with them. We investigated the use of predator conditioning to prepare hellbenders, behaviorally and physiologically, for the presence of a common predator, largemouth bass (Micropterus salmoides). We reared hellbenders for 30 d with and without continuous exposure to largemouth bass kairomones and heterospecific alarm cues and found conditioned hellbenders became less active compared to unconditioned individuals (p = 0.017). After conditioning, we exposed hellbenders to water, a low concentration of kairomones, or a high concentration of kairomones in a closed respirometer system. We measured activity within respirometer chambers and routine metabolic rate. We found unconditioned hellbenders exposed to low and high concentrations of kairomones were 41% and 119% more active than conditioned animals (p = 0.002 and p < 0.001). Moreover, conditioned individuals had on average 6.5% lower metabolic rates across all three kairomone concentrations compared to unconditioned individuals (p = 0.017). Our data suggest that predator conditioning induces behavioral avoidance tactics and physiological changes that could improve future translocation efforts for hellbenders and other imperiled species.

Predators can influence prey directly through consumption or indirectly through nonconsumptive effects (NCEs) by altering prey behavior, morphology, and life history. We investigated whether predator‐avoidance behaviors by larval long‐toed salamanders (Ambystoma macrodactylum) in lakes with nonnative trout result in NCEs on morphology and development. Field studies in lakes with and without trout were corroborated by experimental enclosures, where prey were exposed only to visual and chemical cues of predators. We found that salamanders in lakes with trout were consistently smaller than in lakes without trout: 38% lower weight, 24% shorter body length, and 29% shorter tail length. Similarly, salamanders in protective enclosures grew 2.9 times slower when exposed to visual and olfactory trout cues than when no trout cues were present. Salamanders in trout‐free lakes and enclosures were 22.7 times and 1.48 times, respectively, more likely to metamorphose during the summer season than those exposed to trout in lakes and/or their cues. Observed changes in larval growth rate and development likely resulted from a facultative response to predator‐avoidance behavior and demonstrate NCEs occurred even when predation risk was only perceived. Reduced body size and growth, as well as delayed metamorphosis, could have ecological consequences for salamander populations existing with fish if those effects carry‐over into lower recruitment, survival, and fecundity.

Captive environments are maintained in hygienic ways that lack free-flowing microbes found in animals’ natural environments. As a result, captive animals often have depauperate host-associated microbial communities compared to conspecifics in the wild and may have increased disease susceptibility and reduced immune function. Eastern hellbenders (Cryptobranchus alleganiensis alleganiensis) have suffered precipitous population declines over the past few decades. To bolster populations, eastern hellbenders are reared in captivity before being translocated to the wild. However, the absence of natural microbial reservoirs within the captive environment diminishes the diversity of skin-associated bacteria on hellbender skin and may negatively influence their ability to defend against pathogenic species once they are released into the wild. To prepare hellbenders for natural bacteria found in riverine environments, we devised a novel bioaugmentation method to increase the diversity of skin microbial communities within a captive setting. We exposed juvenile hellbenders to increasing amounts of river water over 5 weeks before translocating them to the river. We genetically identified and phylogenetically compared bacteria collected from skin swabs and river water for alpha (community richness) and beta (community composition) diversity estimates. We found that hellbenders exposed to undiluted river water in captivity had higher alpha diversity and distinct differentiation in the community composition on their skin, compared to hellbenders only exposed to well water. We also found strong evidence that hellbender skin microbiota is host-specific rather than environmentally driven and is colonized by rare environmental operational taxonomic units in river water. This technique may increase hellbender translocation success as increasing microbial diversity is often correlated with elevated disease resistance. Future work is necessary to refine our methods, investigate the relationship between microbial diversity and hellbender health and understand how this bioaugmentation technique influences hellbenders’ survival following translocation from captivity into the wild.