Predator identity and consumer behavior: differential effects of fish and crayfish on the habitat use of a freshwater snail

Predators can alter the outcome of ecological interactions among other members of the food web through their effects on prey behavior. While it is well known that animals often alter their behavior with the imposition of predation risk, we know less about how other features of predators may affect prey behavior. For example, relatively few studies have addressed the effects of predator identity on prey behavior, but such knowledge is crucial to understanding food web interactions. This study contrasts the behavioral responses of the freshwater snail Physellagyrina to fish and crayfish predators. Snails were placed in experimental mesocosms containing caged fish and crayfish, so the only communication between experimental snails and their predators was via non-visual cues. The caged fish and crayfish were fed an equal number of snails, thereby simulating equal prey mortality rates. In the presence of fish, the experimental snails moved under cover, which confers safety from fish predators. However, in the presence of crayfish, snails avoided benthic cover and moved to the water surface. Thus, two species of predators, exerting the same level of mortality on prey, induced very different behavioral responses. We predict that these contrasting behavioral responses to predation risk have important consequences for the interactions between snails and their periphyton resources. Received: 1 June 1998 / Accepted: 12 October 1998     

Fleeing towards death – leech‐induced behavioural defences increase freshwater snail susceptibility to predatory fish

Prey species are often exposed to multiple predators, which presents several difficulties to prey species. This is especially true when the response to one predator influences the prey’s susceptibility to other predators. Predator‐induced defences have evolved in a wide range of prey species, and experiments involving predators with different hunting strategies allow researchers to evaluate how prey respond to multiple threats. Freshwater snails are known to respond to a variety of predators with both morphological and behavioural defences. Here we studied how freshwater snails Radix balthica responded behaviourally to fish and leech predators, both separately and together. Our aim was to explore whether conflicting predator‐induced responses existed and, if so, what effect they had on snail survival when both predatory fish and leeches were present. We found that although R. balthica increased refuge use when exposed to predatory fish, they decreased refuge use when exposed to predatory leeches. When both predators were present, snails showed a stronger response towards leech than fish and responded by leaving the refuge. This response made the snails more susceptible to fish predation, which increased snail mortality when exposed to both fish and leech compared to fish only. We show that predators that have a relatively low predation rate can substantially increase mortality rates by indirect effects. By forcing snails out of refuges such as rock and macrophyte habitats, leeches can indirectly increase predation from molluscivorous fish and may thus affect snail densities.     

Post-translationally modified neuropeptides from Conus venoms.

Predatory cone snails (genus Conus) comprise what is arguably the largest living genus of marine animals (500 species). All Conus use complex venoms to capture prey and for other biological purposes. Most biologically active components of these venoms are small disulfide-rich peptides, generally 7-35 amino acids in length. There are probably of the order of 100 different peptides expressed in the venom of each of the 500 Conus species [1,2]. Peptide sequences diverge rapidly between Conus species, resulting in a distinct peptide complement for each species. Thus, the genus as a whole has probably generated approximately 50 000 different peptides, which can be organized into families and superfamilies with shared sequence elements [3]. In this minireview, we provide a brief overview of the neuropharmacological, molecular and cell-biological aspects of the Conus peptides. However, the major focus of the review will be the remarkable array of post-translational modifications found in these peptides.     

Largemouth bass (Micropterus salmoides) switch feeding modalities in response to sensory deprivation

Animals use a suite of sensory modalities to precisely locate and capture prey. While numerous studies have examined the effects of sensory deprivation on the behaviors leading to prey capture and while it is generally believed that information in the pre-strike period determines the way fish capture prey, this study is the first to examine the contribution of sensory information to jaw kinematics during capture. Largemouth bass were filmed using high-speed videography while capturing live mosquitofish. Bass were examined intact, with visual deprivation under infrared light, and with lateral line deprivation following treatment with cobalt chloride. Deprived of visual cues, this visual ram-feeding predator switches towards suction-based feeding to successfully capture prey. They approach prey slowly but open their mouths more rapidly, which has been shown to result in greater buccal pressure, causing their prey to move a greater distance at a more rapid velocity as they are being drawn into the predators' mouths. Deprived of lateral line cues, bass have higher forward velocities during capture and capture prey earlier in the gape cycle. This study demonstrates that sensory pre-strike information directly affects the capture modality employed by fishes and that fish can modulate between ram and suction not only by adjusting the amount of ram by increasing or decreasing their movements, but also by actively increasing the amount of suction used. These results suggest that the ability to modulate feeding behavior may allow animals to not only exploit a broader breadth of prey items, but also to be capable of doing so in a wider variety of environments.     

Predatory versatility in a larval dragonfly, Hemianax papuensis (Odonata: Aeshnidae)

Larvae of the large dragonfly Hemianax papuensis used four disparate, prey-specific predatory behaviours. Arthropod prey moving on a substratum were stalked and then attacked from a distance. Arthropod prey moving in the water column or at the water surface were approached using 'jet' propulsion and then attacked from a distance. Snails, an unusual prey for an arthropod, were stalked; then the larva manoeuvred about them until a specific orientation was achieved before an attack was made from close range. Dead snails were scavenged, using tactics very similar to those used with live snails, but non-snail carrion was rarely taken. There was no evidence that the possession, by H. papuensis , of specialized behaviours for an atypical prey-snails-lowered its success when attacking other types of 'typical' prey.     

The biological control of snail intermediate hosts of schistosomiasis by fish

Summary The use of molluscivorous fish for biological control of snail intermediate hosts of schistosomiasis is a regularly reappearing theme in the literature on schistosomiasis control. The effectiveness of this control method has not yet been demonstrated, and conclusive field evidence is lacking. In this article the literature on snail control by fish is critically reviewed. Special attention is paid to the cichlid fish Astatoreochromis alluaudi that has been used in well-documented field trials in Kenya and Cameroon. After some small initial success, after a longer period the fish appeared to be ineffective in snail control. Moreover, the fish reproduces at a pace too slow to be of use in large-scale biocontrol trials. Laboratory observations on foraging behaviour and anatomy of the fish give essential cues to explain the failure of the fish in snail control. An observed reduction in the fishes' pharyngeal jaw apparatus, used to crush snails shells, results in a lower profitability of snails. As predicted by a simple foraging model, the prey preference of the fish shifts towards other more profitable prey items, such as benthic and pelagic macrofauna. Although eradication of snails by fish will not be feasible in most cases, the role of natural predators of snails cannot be neglected, and may still be of importance in integrated control efforts.     

Isolation and characterization of a novel conus peptide with apparent antinociceptive activity

Cone snails are tropical marine mollusks that envenomate prey with a complex mixture of neuropharmacologically active compounds. We report the discovery and biochemical characterization of a structurally unique peptide isolated from the venom of Conus marmoreus. The new peptide, mr10a, potently increased withdrawal latency in a hot plate assay (a test of analgesia) at intrathecal doses that do not produce motor impairment as measured by rotarod test. The sequence of mr10a is NGVCCGYKLCHOC, where O is 4-trans-hydroxyproline. This sequence is highly divergent from all other known conotoxins. Analysis of a cDNA clone encoding the toxin, however, indicates that it is a member of the recently described T-superfamily. Total chemical synthesis of the three possible disulfide arrangements of mr10a was achieved, and elution studies indicate that the native form has a disulfide connectivity of Cys1-Cys4 and Cys2-Cys3. This disulfide linkage is unprecedented among conotoxins and defines a new family of Conus peptides.     

Prey preference and gregarious attacks by the invasive flatworm Platydemus manokwari

The flatworm Platydemus manokwari (Tricladida: Rhynchodemidae) preys on various species of land snail, and its introduction to areas outside of its native range is thought to have caused the extinction of native land snails on several Pacific islands. Platydemus manokwari occurs in areas where land snails have been absent since its invasion, suggesting that the flatworm can prey on animals other than land snails. To identify the alternative prey and prey preferences of P. manokwari, I examined the feeding ecology of P. manokwari under field and laboratory conditions. Individuals were observed attacking live earthworms in a forest where land snails are already extinct, on Chichijima, Ogasawara (Bonin) Islands, Japan. I also observed them attacking earthworms and a species of isopod and land snail in the lab. To prey on the worm, similar to other earthworm-eating flatworms, P. manokwari wrapped itself around the prey and fed on it by inserting its pharynx into the earthworm’s body. Large earthworms were able to escape P. manokwari attacks by autotomy, but the autotomized body parts were eaten. Several P. manokwari individuals together attacked earthworms that were larger than themselves. The laboratory experiments showed that such gregarious attacks increased predation success on both large earthworms and land snails. The flatworms also attacked the isopods, although the predation rate was low. These results demonstrate that P. manokwari is a polyphagous predator of slow-moving soil invertebrates (land snails, slugs, earthworms, and isopods) and that invasion by P. manokwari may directly and indirectly impact native soil fauna.     

A novel M-superfamily conotoxin with a unique motif from Conus vexillum

Cone snails are tropical marine mollusks that envenomate prey with a complex mixture of neuropharmacologically active compounds for the purpose of feeding and defence, each evolved to act in a highly specific manner on different parts of the nervous system. Here, we report the peptide purification, molecular cloning, chemical synthesis, and functional characterization of a structurally unique toxin isolated from the venom of Conus vexillum. The novel peptide, designated Vx2, was composed of 21 amino acid residues cross-linked by 3 disulfide bonds (WIDPSHYCCCGGGCTDDCVNC). Intriguingly, its mature peptide sequence shows low level of similarity with other identified conotoxins, and its unique motif (-CCCGGGC-) was not reported in other Conus peptides. However, its signal peptide sequence shares high similarity with those of the M-superfamily conotoxins. Hence, Vx2 could be classified into a new family of the M-superfamily.     

Oral shelling within an adaptive radiation of pupfishes: Testing the adaptive function of a novel nasal protrusion and behavioural preference

Dietary specialization on hard prey items, such as mollusks and crustaceans, is commonly observed in a diverse array of fish species. Many fish consume these types of prey by crushing the shell to consume the soft tissue within, but a few fishes extricate the soft tissue without breaking the shell using a method known as oral shelling. Oral shelling involves pulling a mollusc from its shell and it may be a way to subvert an otherwise insurmountable shell defence. However, the biomechanical requirements and potential adaptations for oral shelling are unknown. Here, we test the hypothesis that a novel nasal protrusion is an adaptation for oral shelling in the durophagous pupfish (Cyprinodon brontotheroides). We first demonstrate oral shelling in this species and then predict that a larger nasal protrusion would allow pupfish to consume larger snails. Durophagous pupfish are found within an endemic radiation of pupfish on San Salvador Island, Bahamas. We took advantage of closely related sympatric species and outgroups to test: (a) whether durophagous pupfish shell and consume more snails than other species, (b) if F1 and F2 durophagous hybrids consume similar amounts of snails as purebred durophagous pupfish, and (c) if nasal protrusion size in parental and hybrid populations increases the maximum size of consumed snails. We found that durophagous pupfish and their hybrids consumed the most snails, but did not find a strong association between nasal protrusion size and maximum snail size consumed within the parental or F2 hybrid population, suggesting that the size of their novel nasal protrusion does not provide a major benefit in oral shelling. Instead, we suggest that the nasal protrusion may increase feeding efficiency, act as a sensory organ, or is a sexually selected trait, and that a strong feeding preference may be most important for oral shelling.     

Feeding on Profitable and Unprofitable Prey: Comparing Behaviour of Growth-Enhanced Transgenic and Normal Coho Salmon (Oncorhynchus kisutch)

We compared the performance of normal and growth hormone‐transgenic coho salmon feeding on surface drifting edible and inedible novel prey items in various social environments. With an inherently higher appetite, we predicted that transgenic fish would be more willing to feed on novel prey, and that visual company with another fish would enhance this difference further. Transgenic and normal fish, of similar size and age, were equally willing to attack both the edible (live insects) and inedible (artificial angling lure flies) prey, but transgenic fish did so faster and were more likely to make repeated attacks. Transgenic fish managed to seize and consume the edible prey after fewer attacks than did normal fish. However, swallowing of prey took longer than for normal fish. More transgenic individuals interacted with the inedible prey compared with normal salmon, and initially, transgenic fish in visual company with another fish also interacted more with the prey than single transgenic or any constellation of normal focal fish. With repeated exposures, the number of individuals attacking and the number of interactions with the prey decreased. These responses were stronger in transgenic fish, partly explained by the initially low response in normal fish. The observed differences are most likely the consequences of elevated levels of growth hormone in transgenic fish generating enhanced feeding motivation and reinforcement capacity. In a natural environment, the performance of a growth hormone‐transgenic fish may therefore depend on the relative abundance of profitable vs. unprofitable prey, as well as the presence of other transgenic individuals.     

Extensive and continuous duplication facilitates rapid evolution and diversification of gene families

The origin of novel gene functions through gene duplication, mutation, and natural selection represents one of the mechanisms by which organisms diversify and one of the possible paths leading to adaptation. Nonetheless, the extent, role, and consequences of duplications in the origins of ecological adaptations, especially in the context of species interactions, remain unclear. To explore the evolution of a gene family that is likely linked to species associations, we investigated the evolutionary history of the A-superfamily of conotoxin genes of predatory marine cone snails (Conus species). Members of this gene family are expressed in the venoms of Conus species and are presumably involved in predator-prey associations because of their utility in prey capture. We recovered sequences of this gene family from genomic DNA of four closely related species of Conus and reconstructed the evolutionary history of these genes. Our study is the first to directly recover conotoxin genes from Conus genomes to investigate the evolution of conotoxin gene families. Our results revealed a phenomenon of rapid and continuous gene turnover that is coupled with heightened rates of evolution. This continuous duplication pattern has not been observed previously, and the rate of gene turnover is at least two times higher than estimates from other multigene families. Conotoxin genes are among the most rapidly evolving protein-coding genes in metazoans, a phenomenon that may be facilitated by extensive gene duplications and have driven changes in conotoxin functions through neofunctionalization. Together these mechanisms led to dramatically divergent arrangements of A-superfamily conotoxin genes among closely related species of Conus. Our findings suggest that extensive and continuous gene duplication facilitates rapid evolution and drastic divergence in venom compositions among species, processes that may be associated with evolutionary responses to predator-prey interactions.     

Neoseiulus californicus (McGregor) and Neoseiulus fallacis (Garman): larval responsesto prey and humidity, nymphal feeding drive and nymphal predation on phytoseiid eggs

Are Neoseiulus californicus (McGregor) and Neoseiulus fallacis (Garman) both specialized predators of spider mites? As part of a series of studies made to answer this question, responses by larvae were assessed in treatments either with or without prey (Tetranychus urticae Koch) and with either moderate or high relative humidities (a factor that may distinguish between these two morphologically similar species). Neoseiulus fallacis larvae had more feeding, ambulatory activity and jerking (intra– or interspecific communication) in all treatments than N. californicus. The percent egg hatch was less and development took longer for N. fallacis larvae than for N. californicus larvae without prey at moderate humidity levels. The nymphs of both mites showed similar drives to feed 1–2>h after being held 12–48 h without food and then given eggs of T. urticae. Neoseiulus californicus nymphs fed more on the eggs of either phytoseiid and thereafter became adults than did N. fallacis nymphs. These data indicate that N. californicus may be a less specialized predator of spider mites than is N. fallacis.     

Sex-specific developmental plasticity of generalist and specialist predatory mites (Acari: Phytoseiidae) in response to food stress

We studied developmental plasticity under food stress in three female-biased size dimorphic predatory mite species, Phytoseiulus persimilis, Neoseiulus californicus, and Amblyseius andersoni. All three species prey on two-spotted spider mites but differ in the degree of adaptation to this prey. Phytoseiulus persimilis is a specialized spider mite predator, N. californicus is a generalist with a preference for spider mites, and A. andersoni is a broad generalist. Immature predators were offered prey patches of varying density and their survival chances, dispersal tendencies, age and size at maturity measured. Amblyseius andersoni dispersed earlier from and had lower survival chances in low density prey patches than N. californicus and P. persimilis. Age at maturity was not affected by prey density in the generalist A. andersoni, whereas both the specialist P. persimilis and the generalist N. californicus accelerated development at low prey densities. Species-specific plasticity in age at maturity reflects opposite survival strategies when confronted with limited prey: to prematurely leave and search for other food (A. andersoni) or to stay and accelerate development (P. persimilis, N. californicus). In all species, size at maturity was more plastic in females than males, indicating that males incur higher fitness costs from deviations from optimal body size.     

An O-conotoxin from the vermivorous Conus spurius active on mice and mollusks

Here, we report the purification, amino acid sequence and a preliminary biological characterization of a peptide, sr7a, from the venom of Conus spurius, a vermivorous species collected in the Yucatan Channel, Mexico. The peptide consists of 32 amino acid residues (CLQFGSTCFLGDDDICCSGECFYSGGTFGICS&; &, amidated C-terminus) and contains six cysteines arranged in the pattern (C-C-CC-C-C) that characterizes the O-superfamily of conotoxins. This superfamily includes several pharmacological families (omega-, kappa-, muO-, delta- and gamma-conotoxins) that target Ca(2+), K(+), Na(+) and pacemaker voltage-gated ion channels. Compared with other O-conotoxins that were purified from venoms, this peptide displays sequence similarity with omega-SVIA (from Conus striatus), delta-TxVIA/B (from Conus textile), omega-CVID (from Conus catus) and kappa-PVIIA (from Conus purpurascens). At a dose of 250 pmol, peptide sr7a elicited hyperactivity when injected intracranially into mice and produced paralysis when injected into the pedal muscle of freshwater snails, Pomacea paludosa, but it had no apparent effect after intramuscular injection into the limpet Patella opea or the freshwater fish Lebistes reticulatus.     

Ontogenetic shifts in intraguild predation on thrips by phytoseiid mites: the relevance of body size and diet specialization

In greenhouse agroecosystems, a guild of spider mite predators may consist of the oligophagous predatory mite Phytoseiulus persimilis Athias-Henriot, the polyphagous predatory mite Neoseiulus californicus McGregor (both Acari: Phytoseiidae) and the primarily herbivorous but facultatively predatory western flower thrips Frankliniella occidentalis Pergande (Thysanoptera: Thripidae). Diet-specialization and the predator body size relative to prey are crucial factors in predation on F. occidentalis by P. persimilis and N. californicus. Here, it was tested whether the relevance of these factors changes during predator ontogeny. First, the predator (protonymphs and adult females of P. persimilis and N. californicus): prey (F. occidentalis first instars) body size ratios were measured. Second, the aggressiveness of P. persimilis and N. californicus towards F. occidentalis was assessed. Third, survival, development and oviposition of P. persimilis and N. californicus with F. occidentalis prey was determined. The body size ranking was P. persimilis females > N. californicus females > P. persimilis protonymphs > N. californicus protonymphs. Neoseiulus californicus females were the most aggressive predators, followed by highly aggressive N. californicus protonymphs and moderately aggressive P. persimilis protonymphs. Phytoseiulus persimilis females did not attack thrips. Frankliniella occidentalis larvae are an alternative prey for juvenile N. californicus and P. persimilis, enabling them to reach adulthood. Females of N. californicus but not P. persimilis sustained egg production with thrips prey. Within the guild studied here, N. californicus females are the most harmful predators for F. occidentalis larvae, followed by N. californicus and P. persimilis juveniles. Phytoseiulus persimilis females are harmless to F. occidentalis.     

Invertebrate vasopressin/oxytocin homologs. Characterization of peptides from Conus geographus and Conus straitus venoms

The vasopressin-oxytocin family of peptides is of very ancient lineage, found in organisms as diverse as hydra and man. Although these peptides have been intensively studied in vertebrates, the presumably more extensive invertebrate series was defined primarily by immunological methods. In this report, we describe the purification and structures of two peptides of the vasopressin-oxytocin family from molluscs ("Conopressins"), which were found in the venom of fish-hunting marine snails of the genus Conus. The biological activity observed when the two snail peptides are injected intracerebrally into mice is very similar to that elicited by the vertebrate neurohypophyseal hormones and presumably reflects their actions upon a common receptor in the brain. The sequences of the purified peptides reveal unique features not found in the vertebrate peptide series, most notably an additional positive charge. These are the first members of the invertebrate series of the vasopressin-oxytocin family to be characterized biochemically. The sequences of these peptides are: from Conus geographus venom, Lys-conopressin-G, Cys-Phe-Ile-Arg-Asn-Cys-Pro-Lys-Gly-NH2; and from Conus striatus venom, Arg-conopressin-S, Cys-Ile-Ile-Arg-Asn-Cys-Pro-Arg-Gly-NH2.     

Developmental modularity and phenotypic novelty within a biphasic life cycle: morphogenesis of a cone snail venom gland

The venom gland of predatory cone snails (Conus spp.), which secretes neurotoxic peptides that rapidly immobilize prey, is a proposed key innovation for facilitating the extraordinary feeding behaviour of these gastropod molluscs. Nevertheless, the unusual morphology of this gland has generated controversy about its evolutionary origin and possible homologues in other gastropods. I cultured feeding larvae of Conus lividus and cut serial histological sections through the developing foregut during larval and metamorphic stages to examine the development of the venom gland. Results support the hypothesis of homology between the venom gland and the mid-oesophageal gland of other gastropods. They also suggest that the mid-region of the gastropod foregut, like the anterior region, is divisible into dorsal and ventral developmental modules that have different morphological, functional and ontogenetic fates. In larvae of C. lividus, the ventral module of the middle foregut transformed into the anatomically novel venom gland of the post-metamorphic stage by rapidly pinching-off from the main dorsal channel of the mid-oesophagus, an epithelial remodelling process that may be similar to other cases where epithelial tubes and vesicles arise from a pre-existing epithelial sheet. The developmental remodelling mechanism could have facilitated an abrupt evolutionary transition to the derived morphology of this important gastropod feeding innovation.     

A field demonstration of the costs and benefits of group living to edible and defended prey

Both theoretical and laboratory research suggests that many prey animals should live in a solitary, dispersed distribution unless they lack repellent defences such as toxins, venoms and stings. Chemically defended prey may, by contrast, benefit substantially from aggregation because spatial localization may cause rapid predator satiation on prey toxins, protecting many individuals from attack. If repellent defences promote aggregation of prey, they also provide opportunities for new social interactions; hence the consequences of defence may be far reaching for the behavioural biology of the animal species. There is an absence of field data to support predictions about the relative costs and benefits of aggregation. We show here for the first time using wild predators that edible, undefended artificial prey do indeed suffer heightened death rates if they are aggregated; whereas chemically defended prey may benefit substantially by grouping. We argue that since many chemical defences are costly to prey, aggregation may be favoured because it makes expensive defences much more effective, and perhaps allows grouped individuals to invest less in chemical defences.