Consequences of competition on the time budgets,growth and distributions of three species of terrestrial slugs

Summary The behavioural time budgets of two non-aggressive slugs and one aggreessive species were evaluated in monocultures or in 2-way combinations in field cages. The seasonal time budgets ofL. maximus, A. ater andA. columbianus in monoculture were remarkably similar despite their strong differences in physiological resource allocation. Similarity in physical design and resource utilization appeared to be more important determinants of behaviour. The time budgets showed distinct seasonal patterns associated with underlying physiological demands for reserve accumulation, sperm acquisition and oviposition.A. ater andL. maximus displayed a definite dispersal phase associated with femalephase maturation. In combination,A. ater andA. columbianus had no detectable effect on one another’s time budgets.L. maximus disrupted nearly every category of behaviour in these non-aggressive species, but its own time budget was not significantly different in the monoculture or in the two combinations, except for minor effects on resting and sexual behaviour.L. maximus appeared to be adapted to maximize behavioural disturbance of interspecific competitors while minimizing intraspecific effects.     

Alternative risk-taking styles: The case of time-budgeting strategies of terrestrial gastropods

The terrestrial slugs Arion ater, Limax maximus and Ariolimax columbianus have similar morphological designs but differ remarkably in their life history tactics and behavioural time budgets. The adaptive value of particular risk-taking styles was investigated using a comprehensive computer simulation model. The model allowed each species' success (growth rates, food acquisition) and costs (distance travelled, hydration deficits, injury from aggressive encounters) to be evaluated in various types of weather (benign, harsh and surprise). This was interpreted in terms of the species' life history design. In addition, each species was simulated with the behavioural strategy of the other two species substituted for its natural programming. The simulation experiments demonstrated how variations in a few simple rules could lead to divergent cost-benefit consequences. The model also illustrated that coarsely-tuned sensitivity to the environment may be better than finely-tuned responses, depending on the animal's ability to respond quickly and the degree of risk. The simulations suggested that competition has shaped the time-budgeting tactics of A. ater and L. maximus. Each species actually performed better in harsh weather, using the behavioural program of the other. L. maximus is an aggressive species with a narrow, nocturnal activity period. The concentrated activity of L. maximus may allow it to displace competitors more effectively, whereas the broader time span of A. ater's activity may be necessary to avoid L. maximus.     

The effects of food and density of the movement ofArion ater andAriolimax columbianus (Pulmonata: Stylommatophora) between habitats

Experiments were conducted to determine if slug density, or food quantity and quality could cause dispersal by slugs. Arion ater dispersed quickly from overcrowded areas, where high mortality was incurred by this species. Poor food conditions, caused more dispersal than good food conditions, but food had no effect on the mortality of A. ater. Neither food nor density factors had significant effects on the dispersal of Ariolimax columbianus. However, more A. columbianus died in the high- than low-density treatments. A. columbianus mortality was unaffected by the food factor. Dispersing Arion were heavier than non-dispersers, but there was no difference between the weights of dispersing and non-dispersing Ariolimax. There were significant seasonal changes in the dispersal rate, mortality and weight of dispersing Arion, whereas only the mortality of Ariolimax changed significantly during the experiments. Since Arion ater did not markedly reduce its activity during unsuitable weather it was able to leave areas of poor food and high slug density fairly rapidly. Ariolimax columbianus' large size allowed it to remain inactive during unfavourable weather and permitted this species to be relatively unresponsive to the experimental treatments.     

Dispersal movements of non-native and native terrestrial slugs in an urban environment

Animal movement varies from undirected dispersal to directed migration. Movement rates may have implications for conservation and resource management, as well as pest control, and they play a key role in invasion success. In slugs, long-distance dispersal is typically passive, whereas active movement is critical for local dispersal and determines access to resources such as food and shelter. Telemetry has recently been used to study individual slug movements in the wild, whereas movement in arena tests has explored mechanisms of interspecific competition and invasiveness in slugs. Studies that relate the performance of individual slugs in arena tests to their post-release behavior in nature are lacking. We measured individual short-term movement speed of commonly occurring native and non-native slugs of the genera Arion and Limax in arena tests and tracked their post-release dispersal movements in a garden by PIT telemetry. We demonstrate clear differences in movement behavior among the species, but non-native slugs did not display higher movement rates than their native congeners. In the arena test, slugs of the genus Limax displayed a higher short-term speed than slugs of the genus Arion, whereas in the field, individuals of Limax maximus showed lower dispersal rates compared to the other slug species. Moreover, there was a positive correlation between short-term speed in the arena test and movement in the field among individuals of L. cinereoniger, indicating the possible existence of behavioral syndromes in slugs, which may link movement ecology, animal personality, and the invasion ecology of pest species.     

The effects of food and density on the nocturnal behaviour ofArion ater andAriolimax columbianus (Pulmonata: Stylommatophora)

The effects of food supply and population density on the nocturnal behaviour of Arion ater and Ariolimax columbianus were investigated. Density did not significantly affect A. ater's level of activity or short-term movement, resting, or feeding. A. columbianus was more active and moved, rested, and fed more frequently when slug density was high. A. ater foraged and rested more often, but fed less when good food was unavailable. Ariolimax's only response to the food regime was to feed more when good food was available. Seasonal changes in the level of activity and behaviour of Arion were evident, whereas Ariolimax's activity and behavioural repertoire were not similarly affected. Arion ater's nightly activity appeared to be mainly food oriented, while Ariolimax columbianus seemed most responsive to slug density during its nocturnal activity periods.     

Immunocytochemical Localisation of Glycosaminoglycan-Like Activity in the Mucus and Associated Tissues of Terrestrial Slug Species (Gastropoda: Pulmonata)

Indirect immunofluorescence assays were conducted on cryotome sections of four terrestrial slug species from three distinct phylogenetic groups, Arion ater (L.), Arion hortensis (Férussac), Tandonia (Milax) budapestensis (Hazay), and Deroceras reticulatum (Müller) using monoclonal antibodies for two glycosaminoglycans (GAGs), heparan sulphate, and chondroitin sulphate. Specific staining for a heparan sulphate-like component was demonstrated in the foot and tail regions of each species and was particularly intense in A. ater and A. hortensis, notably in the epidermis and associated mucus-like material, and in mucus-like material from the pedal gland region of the latter species. Subsequent studies with A. ater confirmed the presence of heparan-sulphate–like activity in the caudal gland duct region. No evidence of specific staining for chondroitin sulphate-like activity was found in any of the slug species. This work suggests that a specific GAG, or a group of closely related GAGs, is a common component of mucus in a range of slug species and of different types of mucus, including trail (pedal) mucus and the more viscous mucus produced by the caudal gland.     

Neurosecretory cells in the central nervous system of the giant garden slug,limax maximumus

The neurosecretory system of the giant garden slug Limax maximus was studied using the alcian blue/alcian yellow (AB/AY) staining technique for neurosecretion. Stainable cells could be identified in the paired cerebral, pleural, parietal, and buccal ganglia, and in the visceral ganglion. The cells occur as single cells or in groups of up to 100, with diameters ranging between 10 and 70 μm. Axon tracts could only be traced for a small number of cells; neurohemal areas were not conclusively identified. The morphological similarities of the neurosecretory system of L. maximus is compared with that of other investigated stylommatophoran slugs.     

Differential antigen decay rates during digestion of molluscan prey by carabid predators

Carabid beetles (Coleoptera: Carabidae) were fed upon slugs (Mollusca: Pulmonata) in the laboratory, and their crop contents analysed for mollusc remains, using an enzyme-linked immunosorbent assay (ELISA) with an anti-Arion ater (L.) haemolymph antiserum. Crop weight loss and antigenic recognition of prey proteins were examined as separate variables in a series of validatory experiments. Two model predators,Abax parallelepipedus Piller and Mitterpacher andPterostichus madidus F., were fed upon two species of pest slugs,Deroceras reticulatum (Müller) andArion hortensis Férussac. The fitting of regression equations to the transformed antigenic response data allowed the ‘half-life’ and detection period to be calculated for each predator-prey combination. Following a one hour feeding interval, the half-life of the antigenic response toD. reticulatum remains was almost twice as long inP. madidus as that inA. parallelepipedus, and the detection period more than 2.5 times as long. However, covariant analysis showed that there was a significant difference between predator species in the rate at which detectability declined, but not in the rate of crop weight loss. WhenA. parallelepipedus was allowed to feed uponA. hortensis for eight hours, prey remains were still detectable at the end of the experiment, 13 days after feeding. Calibration of the differential rates of antigen decay and crop weight loss could potentially be used to calculate the size of the original meal, but only if prey species, and the time since feeding, can be determined. Potential solutions to these problems are discussed.     

Association of Entomopathogenic Fungi with Exotic Bark Beetles in New Zealand Pine Plantations

Hylastes ater and Hylurgus ligniperda are introduced pests of re-established Pinus radiata in New Zealand. Both species breed under the bark of stumps in recently harvested areas. Adult maturation feeding on pine seedlings planted in adjacent areas can significantly impact seedling growth, and in severe cases seedlings will die. Entomopathogenic fungi are important natural mortality factors in bark beetle populations, and Beauveria spp. are predominant. Here, we report on the isolation of other fungal species from H. ater in New Zealand. Based on morphological characteristics and sequencing data, two species, Metarhizium flavoviride var. pemphigi and Hirsutella guignardii, were recovered from H. ater. Both are new records for New Zealand and appear to be the first records of these species from bark beetles worldwide.     

r-and K-selection in soil ciliates: a field and experimental approach

Summary Previously published field studies have suggested that the concept of r/K selection may be applied to terrestrial ciliates. A census was taken of the dominant groups, the Colpodea and Polyhymenophora, to determine species composition and absolute abundances in climatically unpredictable alpine and predictable lowland sites. In addition, two typical representatives of each of the two taxa (Colpoda aspera and Grossglockneria acuta, and Blepharisma undulans and Gonostomum affine, respectively) were selected for examination under laboratory conditions. Variables investigated were: the C/P index (ratio of Colpodea to Polyhymenophora), fertility, tolerance of altered environmental conditions, incidence in predictable or unpredictable biotopes, opportunism, competitive ability, and body size. Our own observations were supplemented by reference to the literature.The field census produced a higher C/P index in the unpredictable sites than in the predictable ones. The experiments show that C. aspera and G. acuta are less sensitive to changes in temperature and exhibit a more rapid rise in individual density as well as a higher number of individuals than do B. undulans and G. affine, although the former species have longer generation times at low temperatures. The explosive increase in number of individuals can be ascribed to the special reproductive strategy of the Colpodea (quadripartition in cysts). These results imply that the Colpodea are more r-selected as compared with the Polyhymenophora. That might be an explanation for their wide distribution and high density in unfavourable terrestrial habitats.     

Restoration impacts on fuels and fire potential in a dryland tropical ecosystem dominated by the invasive grass Megathyrsus maximus

Ecological restoration often attempts to promote native species while managing for disturbances such as fire and non‐native invasions. The goal of this research was to investigate whether restoration of a non‐native, invasive Megathyrsus maximus (guinea grass) tropical grassland could simultaneously promote native species and reduce fire potential. Megathyrsus maximus was suppressed with herbicide, and three suites of native species—each including the same groundcover and shrub, and one of three tree species—were outplanted in a randomized, complete block design that also included herbicide control (herbicide with no outplantings) and untreated control treatments. Fuels were quantified 27 months after outplanting, and potential fire behavior (rate of spread and flame length) was modeled with BehavePlus. Compared with untreated controls, native outplant treatments reduced M. maximus cover by 76–91% and M. maximus live and dead fuel loads by greater than 92 and 68%, respectively. Despite reductions in M. maximus fuels, neither treatment‐level (grass + native) total fuel loads and fuel moistures, nor modeled fire behavior differed between outplant treatments and controls. The best performing native woody species (Dodonaea viscosa) had significantly lower average individual plant live fuel moisture (84%) than M. maximus (156%) or other native woody outplant species (201–328%), highlighting the need for careful species selection. These results demonstrate that restoring native species to degraded tropical dry forests is possible, but that ecological restoration will not necessarily alter the potential for fire, at least in the short term, making selection of species with beneficial fuel properties and active fire management critical components of ongoing restoration.     

Cold tolerance and freeze-induced glucose accumulation in three terrestrial slugs

Cold tolerance and metabolic responses to freezing of three slug species common in Scandinavia (Arion ater, Arion rufus and Arion lusitanicus) are reported. Autumn collected slugs were cold acclimated in the laboratory and subjected to freezing conditions simulating likely winter temperatures in their habitat. Slugs spontaneously froze at about − 4 °C when cooled under dry conditions, but freezing of body fluids was readily induced at − 1 °C when in contact with external ice crystals. All three species survived freezing for 2 days at − 1 °C, and some A. rufus and A. lusitanicus also survived freezing at − 2 °C. ¹H NMR spectroscopy revealed that freezing of body fluids resulted in accumulation of lactate, succinate and glucose. Accumulation of lactate and succinate indicates that ATP production occurred via fermentative pathways, which is likely a result of oxygen depletion in frozen tissues. Glucose increased from about 6 to 22 μg/mg dry tissue upon freezing in A. rufus, but less so in A. ater and A. lusitanicus. Glucose may thus act as a cryoprotectant in these slugs, although the concentrations are not as high as reported for other freeze tolerant invertebrates.     

Invasive slugs as under-appreciated obstacles to rare plant restoration: evidence from the Hawaiian Islands

Introduced slugs have invaded many parts of the world where they were recognized as important pests of gardens and agriculture, but we know little about the effects of introduced slugs on rare plants in natural areas. The Hawaiian Islands have no native slugs, but over a dozen introduced slug species are now established. We reviewed Rare Plant Recovery Plans produced by the U.S. Fish and Wildlife Service for Hawaii and found that introduced slugs were specifically mentioned as threats or potential threats to 59 rare plant species (22% of all endangered and threatened plants), based mainly on anecdotal observations by field biologists. We then initiated an experimental field study to assess the impact of slug herbivory on the growth and survival of two endangered plant species (Cyanea superba, and Schidea obovata), one non-endangered native species (Nestegis sandwicensis) and two co-occurring invasive plant species (Psidium cattleianum and Clidemia hirta). In mesic forest on the Island of Oahu, we tracked the fate of outplanted seedlings in replicated 1 m² plots, with and without slug control. Slugs decreased seedling survival of the endangered species by 51%, on average. Slugs did not significantly affect survival of the non-endangered or invasive plant species. Introduced slugs seem to be under-appreciated as a direct cause of plant endangerment. Invasive slugs may also facilitate the success of some invasive plant species by reducing competition with more palatable, native plant competitors. Slug control measures are relatively inexpensive and could facilitate rare plant establishment and population recovery.     

Predation by the carabid beetles Pterostichus madidus and Nebria brevicollis is affected by size and condition of the prey slug Deroceras reticulatum

1 Slugs are important pests in many agricultural crops but molluscicides commonly used to control slugs affect non‐target organisms. Encouraging biological control may help to reduce molluscicide use, but the efficiency of potential natural enemies needs to be investigated. 2 Serological tests have shown that certain carabid species consume slugs. These techniques, however, do not distinguish between scavenging and true predation, nor do they provide information on the size or other characteristics of the prey consumed. The study reported here was undertaken to establish whether scavenging of dead slugs might be an important factor contributing to positive serological test results. 3 Both Pterostichus madidus (Fabricius) and Nebria brevicollis (Fabricius) consumed Deroceras reticulatum (Müller) under laboratory conditions. Dead slugs were scavenged in preference to injured or healthy slugs. 4 Only small, live slugs (< 0.11 g) were killed by both beetle species, which may, therefore, be incapable of killing larger slugs. 5 These generalist beetle species appeared unable to overcome the defence mucus produced by slugs. The data suggest that positive serological results from field collected beetles may reflect scavenging rather than predation on live or injured slugs.     

Competition between Native Hawaiian Plants and the Invasive Grass Megathyrsus maximus: Implications of Functional Diversity for Ecological Restoration

Biodiversity loss is a global crisis, due primarily to habitat destruction and widespread nonnative invasions. Invasive grasses are particularly problematic in many tropical ecosystems, where they possess traits that promote their persistence and can drastically alter native plant communities. We explored the ecophysiological basis for restoring native Hawaiian dryland ecosystems currently dominated by the nonnative invasive grass Megathyrsus maximus (guinea grass) in a garden experiment. Three native species—Myoporum sandwicense (naio; canopy tree), Dodonaea viscosa (aalii; shrub), and Plumbago zeylanica (iliee; groundcover)—were grown with M. maximus at three levels of native functional diversity (one, two, or three species) while holding overall plant density constant. We tested which individual and functional combinations of native species were more productive and best suppressed M. maximus growth and reproduction. Megathyrsus maximus had 39–94% higher maximum photosynthetic rates (A_max) than native species and increasing native functional diversity did not affect M. maximus A_max. Aboveground, belowground, and total biomass of M. maximus varied with functional diversity, although intraspecific competition reduced growth as much as interspecific competition. Reproductive tiller production by M. maximus decreased significantly when planted with any of the native species and with increasing native functional diversity. These results indicate that high native functional diversity in an ecological restoration setting may aid in the control of a dominant invasive grass and the reintroduction of diverse native species. Recommendations for restoring degraded nonnative grasslands in Hawaii and throughout the tropics include selection of native species that are ecophysiologically competitive and have high functional diversity.     

Do pioneers have r-selected traits? Life history patterns among colonizing terrestrial gastropods

We examine whether pioneer species of terrestrial gastropods (snails and slugs) possess particular life history traits commonly associated with r-selection, using data on gastropod colonization in four areas in north-west Europe (the Kvarken and Tvärminne archipelagos in the Baltic, polder woods in IJsselmeer, and a rehabilitated quarry near Maastricht). Data on age at first reproduction, longevity, clutch size, egg size and lifetime fecundity were gathered from the literature. In order to control for potentially confounding effects of body size on life history traits, we compared the residuals from the allometric relations between life history traits and body size for pioneers and non-pioneers. In snails, all life history traits examined were related to body size. In slugs, all traits except age at first reproduction scaled with body size. Body sizes did not differ between pioneers and non-pioneers in any area. In all four areas, there were no significant differences between pioneers and non-pioneers in any of the life history traits examined, after body size had been taken into account. This indicates that pioneer terrestrial gastropods generally cannot be regarded as r-selected. Pioneer species may possess any of several life history strategies, and the combinations of traits shown by them may have little in common with the r-K selection concept.     

Fish predation and offspring survival in the prosobranch snail Viviparus ater

In this study we identified some of the predators of the freshwater snail Viviparus ater and estimated offspring survival to the end of the first summer in a natural population. Newborn V. ater were eaten by the fish Barbus barbus, Rutilus rutilus, Scardinius erythrophtalmus and Tinca tinca. Out of 137 guts of Abramis brama caught in Lake Zürich 1 contained shell fragments and an operculum of a newborn V. ater. On a 40×40 m grid near Goldbach, Lake Zürich, we counted 678 adult females of V. ater in June 1988, which together gave birth to approximately 13 300 offspring throughout the summer. In October we found 1348 V. ater of age class 0 on the grid, i.e. approximately 10% of the year's young had survived to the end of their first summer. The grid had been divided into two sections, A and B. In section A, 72 carthenware tiles had been placed as shelters for V. ater. Offspring survival was slightly but significantly higher here (10.9%) than in section B (9.6%). The observation that offspring survival in the natural habitat was 1 order of magnitude lower than in cages suggests that predation is an important cause of mortality of newborn V. ater. Average population density was 2 individuals m^–2 There was a migration from shallow (1–4 m) to deeper water (5–9 m) in September. The average distance between weekly recordings of tagged V. ater was 4.7 m in males and 3.0 m in females.     

Exotic Slugs Pose a Previously Unrecognized Threat to the Herbaceous Layer in a Midwestern Woodland

Developing effective restoration strategies requires first identifying the underlying factors limiting native plant recovery. The slug Deroceras reticulatum is an important herbivore in Europe, a global agricultural pest, and is introduced and abundant throughout eastern North America, but little information is available on the effect of this exotic herbivore on the forest herbaceous layer. Here, we test the palatability of 12 forest herbs to the introduced slug D. reticulatum and use field surveys to determine the degree to which slugs are damaging plants in the field. In laboratory feeding trials, slugs readily consumed most plants, but avoided the grass Elymus virginicus, the invasive forb Alliaria petiolata (garlic mustard), and thicker leaved plants. In the field, we documented significant slug damage, with close to 50% or more of plant leaves damaged by slugs on five of the six native species tested. Slug damage in the field was predicted by laboratory‐determined acceptability, but was significantly greater on short‐statured rosette species than on erect plants for a given acceptability value. Our results identify introduced slugs as an important, but overlooked obstacle to forest herb restoration and potential drivers of larger scale understory compositional change. The relaxed herbivore pressure on A. petiolata, relative to native competitors, suggests that invasive plant removal alone may not result in the recovery of native flora. Rather, restoration of unpalatable native species should accompany invasive plant control in slug invaded areas. Erect forbs, thick‐leaved plants, and graminoids should have the greatest success where introduced slugs are abundant.