Parasite-mediated predation between native and invasive amphipods

Parasites can structure biological communities directly through population regulation and indirectly by processes such as apparent competition. However, the role of parasites in the process of biological invasion is less well understood and mechanisms of parasite mediation of predation among hosts are unclear. Mutual predation between native and invading species is an important factor in determining the outcome of invasions in freshwater amphipod communities. Here, we show that parasites mediate mutual intraguild predation among native and invading species and may thereby facilitate the invasion process. We find that the native amphipod Gammarus duebeni celticus is host to a microsporidian parasite, Pleistophora sp. (new species), with a frequency of infection of 0-90%. However, the parasite does not infect three invading species, G. tigrinus, G. pulex and Crangonyx pseudogracilis. In field and laboratory manipulations, we show that the parasite exhibits cryptic virulence: the parasite does not affect host fitness in single-species populations, but virulence becomes apparent when the native and invading species interact. That is, infection has no direct effect on G. d. celticus survivorship, size or fecundity; however, in mixed-species experiments, parasitized natives show a reduced capacity to prey on the smaller invading species and are more likely to be preyed upon by the largest invading species. Thus, by altering dominance relationships and hierarchies of mutual predation, parasitism strongly influences, and has the potential to change, the outcome of biological invasions.     

An acanthocephalan parasite mediates intraguild predation between invasive and native freshwater amphipods (Crustacea)

1. The balance of predation between closely related invasive and native species can be an important determinant of the success or failure of biological invasions. In Irish freshwaters, the introduced amphipod Gammarus pulex has replaced the native G. duebeni celticus, possibly through differential mutual intraguild predation (IGP). Theoretically, parasitism could mediate such predation and hence the invasion outcome. However, this idea remains poorly studied. 2. In a field survey, we show that the acanthocephalan parasite Echinorynchus truttae is present in more G. pulex populations than G. d. celticus populations. In addition, within parasitised populations, E. truttae is more prevalent in the invader than in the native. 3. We show for the first time that an acanthocephalan parasite mediates predation between its intermediate macroinvertebrate hosts. In a field experiment, E. truttae parasitism of the invader lowered IGP upon the unparasitised native. In laboratory experiments, parasitism of G. pulex significantly reduced their predatory impact on recently moulted female G. d. celticus. Parasitism also appeared to cause reduction in predatory behaviour, such as attacks per contact on precopula guarded female natives. 4. We conclude that higher parasite prevalence in invaders as compared with natives, by mediation of interspecific interactions, could promote species coexistence, or at least slow species replacements, in this particular biological invasion.     

Comparison of the functional responses of invasive and native amphipods

While we can usually understand the impacts of invasive species on recipient communities, invasion biology lacks methodologies that are potentially more predictive. Such tools should ideally be straightforward and widely applicable. Here, we explore an approach that compares the functional responses (FRs) of invader and native amphipod crustaceans. Dikerogammarus villosus is a Ponto-Caspian amphipod currently invading Europe and poised to invade North America. Compared with other amphipods that it actively replaces in freshwaters, D. villosus exhibited significantly greater predation, consuming significantly more prey with a higher type II FR. This corroborates the known dramatic field impacts of D. villosus on invaded communities. In another species, FRs were nearly identical in invasive and native ranges. We thus propose that if FRs of other taxa and trophic groups follow such general patterns, this methodology has potential in predicting future invasive species impacts.     

Parasite-mediated intraguild predation as one of the drivers of co-existence and exclusion among invasive and native amphipods (Crustacea)

Parasitism is emerging as one of the forces determining the outcome of biological invasions. Using field survey and laboratory experiments, we investigate parasitism as one of the factors mediating the interactions among invasive and native amphipods. An extensive survey (100 sites) of a small British island, revealed the native Gammarus duebeni celticus to be parasitised by the muscle wasting microsporidian Pleistophora mulleri and the acanthocephalan duck parasite Polymorphus minutus, the introduced European Gammarus pulex only by P. minutus and the North American Crangonyx pseudogracilis by neither. While Gammarus spp. were widespread in rivers (one or both species present in 64% of sites), C. pseudogracilis had a restricted distribution (7% of sites) and always co-occurred with Gammarus spp. In contrast, Gammarus spp. were absent from all pond/reservoir sites, with C. pseudogracilis present in over 90%. While the negative association of C. pseudogracilis with Gammarus spp. undoubtedly results from factors such as physico-chemical tolerance and predation as C. pseudogracilis can be heavily predated by Gammarus spp., it was notable that C. pseudogracilis co-occurred with Gammarus spp. more frequently when the latter were parasitised. Laboratory experiments clearly showed that predation on C. pseudogracilis was greatly diminished when G. d. celticus was parasitised by P. mulleri and G. pulex by P. minutus. Our study provides evidence that parasitism, by mediating a key interspecific interaction, is one of an array of interacting factors that may have a role in driving patterns of exclusion and co-existence in natives and invaders.     

Short-term predator avoidance behavior by invasive and native amphipods in the Great Lakes

Understanding predator avoidance behavior by prey remains an important topic in community and invasion ecology. Recently, the Ponto-Caspian amphipod Echinogammarus ischnus (Stebbing 1898) was accidentally introduced into the Great Lakes. Since its introduction, it has displaced the native amphipod, Gammarus fasciatus (Say 1818), from several locations in the lower lakes. To assess whether behavioral differences in predator avoidance might be a causal mechanism increasing the success of the invasive amphipods, two experiments were conducted examining (1) native and invasive amphipod behavioral responses to five fish species with different foraging behaviors, and (2) amphipod responses to different densities of round gobies, a hyper-abundant benthic invertivore. Echinogammarus reduced its distance moved in the presence of all fish species tested, whereas Gammarus reduced its distance moved only after exposure to round gobies, black crappies, and rainbow darters. Both amphipod species increased the time spent motionless following exposure to round gobies, but not after encountering the scent of most of the remaining fish predators. The exception was that Echinogammarus also responded to black crappie scent whereas Gammarus did not. Although both amphipod species exhibited behavioral responses to many of the fish predators, the magnitude of their responses differed only after exposure to the brown bullhead. In the bullhead trials, Echinogammarus reduced its distance traveled significantly more than Gammarus. Both amphipod species increased their avoidance response to increasing goby density, however, the pattern of avoidance behavior was different. Invasive E. ischnus exhibited a consistently strong avoidance response to round gobies over the test duration. Native G. fasciatus initially avoided goby scent, but then either ceased their avoidance response or showed a hyper-avoidance response, depending on goby density. These results suggested (1) both species of amphipods were able to differentiate and react to a variety of fish predators, (2) invasive Echinogammarus amphipods avoided a larger range of fish predators than the native Gammarus, (3) increased avoidance behavior was associated with an increased density of fish, and (4) the avoidance response patterns of invasive Echinogammarus when faced with round goby predators might lead to increased predation on native Gammarus in habitats where they co-occur.     

Silent assassins: predation of native New Zealand trichopteran eggs by non-native freshwater gastropods

Aquatic insects that oviposit on rocks may evolve strategies to mitigate loss of eggs to opportunistic predation by common native grazers, but such strategies may be ineffective against non-native grazers. We tested whether the eggs of common New Zealand caddisfly families (Hydrobiosidae and Hydropsychidae) that oviposit on rocks were more susceptible to predation by native or non-native snails. The native snail Potamopyrgus antipodarum (Grey, 1843) and non-native snails Physa acuta Draparnaud, 1805 and Pseudosuccinea columella (Say, 1817) were presented with caddisfly egg masses and the number of individual eggs consumed was recorded after 24 and 48 hours. The larger Pseudosuccinea readily consumed the eggs, especially spumaline-encapsulated Hydrobiosidae eggs. Physa consumed very few Hydrobiosidae eggs and no Hydropsychidae eggs, whereas Potamopyrgus did not consume eggs of either family. The trichopteran egg masses tested did not succumb to predation by the native Potamopyrgus but are highly vulnerable to predation by a larger non-native snail.     

Laboratory evaluation of predation on mosquito larvae by Australian mangrove fish

A series of laboratory experiments compared predation rates of three native eastern Australian mangrove fish species (Psuedomugil signifer, Hyseleotris galii, Pseudogobius sp.) and the exotic Gambusia holbrooki on 2^nd and 4^th instar Aedes vigilax larvae, in order to determine their potential as mosquito control agents in mangrove forests. All four species preyed on significant numbers of both 2^nd and 4^th instar larvae. All showed a similar pattern of larval consumption, gorging on larvae in the first hour of each experiment, before reducing to a relatively constant background feeding rate. Gambusia holbrooki showed the highest larval consumption rates, but is unsuitable as a mosquito control agent due to it being an exotic pest species in Australia. Of the three native species, P. signifer showed the greatest potential as a mosquito control agent, having consumption rates comparable to G. holbrooki, and was the only species that did not show a significant reduction in larval consumption in the night experiments.     

Studies on predation on mosquito larvae by the fish macropodus cupanus

Maximum Reactive Distance (RD_max) and the area of the Reactive Perceptual Field (RPF) for the fish Macropodus cupanus were determined, using the fourth instar mosquito larva (Culex fatigans) as the prey organism. RD_max and the area of RPF increased with increasing body weight of the fish as well as increasing food deprivation time. Satiation time (St) as a function of the weight of the fish and aquarium temperature were also determined. In larger W classes (570 and 270 mg) St was not influenced by temperature. To get satiated the smallest W class (80 mg) required feeding periods of 40, 30 and 20 minutes at 22 or 27, 32 and 37°C, respectively.     

Ecological and evolutionary significance of cyclopoid predation on fish larvae

Of 412 cyclopoids found preying on fish larvae in Lake Michigan,411 were adult females. It is suggested that adult, female cyclopoidpredation on fish larvae may represent an important mechanismboth to reduce intraspecific competition for food (i.e. betweensexes) and maximize net energy intake for reproduction. Ourobservations of cyclopoid predation on fish larvae in naturemay also provide complementary evidence on how freshwater parasiticcyclopoids evolved from free-living ancestors. Freshwater, parasiticcyclopoids may have evolved from an ancestral free-living cyclopoidwhich was predaceous on small organisms, to a free-living cyclopoid(e.g. Acanthocyclops vernalis and Diacyclops thomasi) whichwas predaceous on larger prey such as fish larvae. Evolutionthen could have proceeded to a free-living cyclopoid with intermediatemorphological modification of its second antennae (e.g. Ergasiluschautauquaensis), and finally to a parasitic cyclopoid whichmorphologically exhibits a high degree of modification in itssecond antennae (e.g. many species of Ergasilus).     

A marking technique for live fish eggs and larvae

 A new marking technique for live fish eggs and larvae was proposed to elucidate the larval biology and adult breeding ecology of wild fish. In the laboratory, females of a freshwater goby Rhinogobius sp. OR were abdominally injected with one of three coloring agents—brilliant blue FCF, rose Bengal, or β-carotene—before their oviposition. The rose Bengal proved lethal to adult fish. The other two dyes had little effect on adult mortality. With these two treatments, there were negative effects on neither fecundity nor egg mortality, resulting in normally developed larvae. The brilliant blue FCF stained eggs and larvae greenish blue whereas the staining effect of β-carotene was unclear. The timing of injection was important in effective staining of eggs and reducing the risk of miscarriage. In conclusion, the brilliant blue FCF was the more useful marker. We discuss what this method can show us about the ecology of wild fish and how this method can be applied to field study. Received: March 6, 2002 / Revised: July 11, 2002 / Accepted: August 14, 2002 RID="*" ID="*" Present address: Center for Marine Environmental Studies, Ehime University, 3 Bunkyo-cho, Matsuyama 790-8577, Japan (e-mail: nokuda@sci.ehime-u.ac.jp) Acknowledgments I am grateful to K. Karino, M. Kohda, and A. Moriyama for giving us valuable advice and to M. Inoue and H. Miyatake for their field assistance. This study was financially supported by Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists. Correspondence to:Noboru Okuda     

Size matters: predation risk and juvenile growth in North Island brown kiwi (

This study investigated how predation risk in North Island brown kiwi changes as the birds grow and develop. Over a 10-year period, 53 adult and 126 young kiwi were radio-tagged at Lake Waikaremoana and studied to determine survival rates, causes of death, and rates of growth. Predation loss amongst adults was low (2.49% year^-1) and caused mainly by ferrets. Young kiwi suffered intense predation from stoats during their first four months of life, but thereafter became too large (> 800 g) for stoats to kill. Juveniles took at least 880 days to attain adult size, about four times longer than expected for a 2–3 kg bird. Growth rates peaked at about the point of hatch, rather than later on in development as in other birds. We suggest that a long evolutionary history dominated by resource limitation rather than predation may account for slow rates of development in kiwi, and that differences among kiwi species in their ability to persist in the presence of stoats are explained by differences in the time that they take to reach safe-size.     

Ocean acidification increases the vulnerability of native oysters to predation by invasive snails

There is growing concern that global environmental change might exacerbate the ecological impacts of invasive species by increasing their per capita effects on native species. However, the mechanisms underlying such shifts in interaction strength are poorly understood. Here, we test whether ocean acidification, driven by elevated seawater pCO₂, increases the susceptibility of native Olympia oysters to predation by invasive snails. Oysters raised under elevated pCO₂ experienced a 20% increase in drilling predation. When presented alongside control oysters in a choice experiment, 48% more high-CO₂ oysters were consumed. The invasive snails were tolerant of elevated CO₂ with no change in feeding behaviour. Oysters raised under acidified conditions did not have thinner shells, but were 29–40% smaller than control oysters, and these smaller individuals were consumed at disproportionately greater rates. Reduction in prey size is a common response to environmental stress that may drive increasing per capita effects of stress-tolerant invasive predators.     

Effects of coexistence on habitat use and trophic ecology of interacting native and invasive amphipods

1. Invasive species in aquatic systems are major drivers of changes in biodiversity. Amphipods are key species in freshwaters, with invasive amphipods either replacing or coexisting with native species and often damaging local biodiversity. However, the consequences of interactions among native and invasive amphipods for their habitat use and feeding ecology and ecosystem function are not yet well understood. 2. We examined a number of streams in Brittany and Northern Ireland, with native and invasive amphipods, to evaluate the consequences of species interactions for both habitat use and diet. Our field studies centred on testing two proposed models: a cohabitation model without competition between two native species (Gammarus pulex vs Echinogammarus berilloni), and a competition model between an invasive and a native species (Gammarus pulex vs Gammarus duebeni celticus). For these three species, alone and in combination, we assessed their habitat use and feeding patterns, the latter through gut contents and stable C and N isotope analyses of their tissues. 3. When existing as single‐species populations, all three species used stream habitats broadly similarly, although G. pulex was more strongly associated with leaf litter and vegetation compared to pebble substrata than the other species. When G. pulex coexisted with either E. berilloni or G. d. celticus, the latter two changed to using all habitats equally, whereas the former retained its habitat preferences. 4. Similarly, all three species when alone had similar gut contents, with inorganic material predominating, followed by leaf and woody material and more rarely algae and invertebrates. When G. pulex coexisted with E. berilloni, the diet of the latter did not change; however, the frequency of inorganic matter, leaves and wood declined in the gut contents of G. pulex. When G. pulex coexisted with G. d. celticus, the pattern of gut contents did not change in either species. 5. When existing as single‐species populations, G. pulex had a broader range of isotopic signatures, both for δ¹³C and for δ¹⁵N, than the two other species, indicating a more variable diet among individuals. When G. pulex coexisted with either E. berilloni or G. d. celticus, the latter two had similar ranges of δ¹³C and δ¹⁵N, whereas for G. pulex the range was much less for δ¹³C and δ¹⁵N, suggesting a less diverse diet. 6. Our results infer two different modes of coexistence between native and non‐native amphipods. We have shown that the native species, which coexist stably, appear to show interference competition, leading to spatial habitat segregation, whereas competition for food and possible intraguild predation by G. pulex on G. d. celticus would explain why the distribution and density of the latter is affected by G. pulex. However, since all the species have a similar diet and feeding habit, we expect no great overall effect on ecosystem processes as a consequence of species interactions and displacements.     

High invasive ant activity drives predation of a native butterfly larva

Yellow crazy ants (Anoplolepis gracilipes) threaten invertebrates on many tropical islands, but little work has been done in continental ecosystems. We found 4.4–16.0 times more cruiser butterfly caterpillars were attacked in Australian rain forest sites with A. gracilipes than in native ant sites, and extrafloral nectar had little influence.     

Chemical protection of Calvia quatuordecimguttata eggs against intraguild predation by the invasive ladybird Harmonia axyridis

Intraspecific and interspecific predation of eggs is a well documented phenomenon amongst aphidophagous coccinellids. The invasive species Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is known to be a top intraguild predator and reported to attack the eggs of many coccinellid species both in a laboratory setting and in the wild. A previous laboratory study highlighted that while many species’ eggs were highly palatable to H. axyridis, the eggs of Calvia quatuordecimguttata (Linnaeus) (Coleoptera: Coccinellidae) appeared to be extremely well protected from attack. Here we present the results of behavioural experiments testing the hypothesis that substances on the egg surface are responsible for this protection, and report preliminary results of GC-MS analysis of these compounds. When the coatings of C. quatuordecimguttata eggs were removed using hexane, they became significantly more susceptible to predation by neonate H. axyridis larvae. However, their overall palatability was not affected, in that complete consumption was never or rarely observed. This suggests that the surface compounds are a true indicator of unpalatability in this species. The effect of hexane-washing on already palatable conspecific eggs was also analysed but had no significant effect on the susceptibility of eggs to cannibalism. We conclude that the eggs of at least one European species are effectively protected by surface deterrents from intraguild predation by H. axyridis. This effect might be due to both the diversity and abundance of hydrocarbons present within the egg coating, the presence of alkenes and/or the presence of patches of a red substance on the eggs’ surface, which is thought to belong to the acid group. In conjunction with data on the susceptibility of other immature stages of C. quatuordecimguttata, this finding may indicate a decreased risk of the species falling victim to invasive H. axyridis, despite their coincident habitat ranges.     

Caddis larvae (Trichoptera) as predators of fish eggs

SUMMARY. Eggs of bullhead ( Cottus gobio ) were found with damaged shells and with the contents removed. Experiments in laboratory aquaria indicated that the damage was caused by caddis larvae and that the type of caddis involved in egg predation might be identified by the nature of the shell damage.     

Interference competition among native and invader amphipods

Aquarium experiments were used to study indications of interference competition, such as substratum choice shifts, swimming activities and mortality of invasive and indigenous gammarids in each other's presence. The more recent invaders Gammarus tigrinus and Dikerogammarus villosus were more likely to prefer stone substratum, whereas the native Gammarus pulex and an earlier invader Gammarus roeseli were found more frequently in the water layer. Sand was the least likely substratum to be chosen by any of the species. G. pulex and G. roeseli did not alter their substratum preference in each other's presence. In the presence of D. villosus, G. pulex shifted towards smaller stones and increased its swimming activities, whereas D. villosus did not change its behaviour in the presence of G. pulex. These shifts may indicate interference competition, with D. villosus being the stronger competitor. The greatest shifts in substratum preference arose when one species had occupied a substratum before the other one was introduced, especially when D. villosus was already present before G. pulex was introduced, possibly indicating pre-emptive competition. Swimming activities of G. pulex increased in the presence of D. villosus, whereas D. villosus spent little time swimming. Mortality was comparable between the different experiments without any indication of predation. The effect of Intra Guild Predation (IGP) may not be reflected adequately by short-time experiments as moults occurred seldom during the experiments. Although no IGP was observed during our experiments, habitat shifts occurred, which may indicate that competitive interactions are apparent before IGP starts. Such shifts may serve to avoid intraguild competition.     

Comparison of sleds versus plankton nets for sampling fish larvae and eggs

Fish larvae and fish eggs were sampled from the inshore waters of eastern Lake Michigan from 1978 through 1980, using a benthic sled and a plankton net towed within 0.5 m of the lake bottom. Differences between estimates of ichthyoplankton abundance based on the benthic sled and those based on the plankton net towed near bottom were examined along with interactions between gear, bottom depth, and time of day. Time of day was determined to be an important factor in comparing these two gear, but data were inconclusive as to the effect of depth on gear differences. Abundance of fish eggs calculated using sled tow data was significantly higher than that for the plankton net. For nighttime collections, density of alewife Alosa pseudoharengus larvae sampled in the plankton net significantly exceeded that for the sled, whereas density of spottail shiner Notropis hudsonius larvae based on sled data was significantly higher than that based on the plankton net for day sampling. Overall, the plankton net appeared to be adequate for sampling abundance of alewife larvae, while the sled was preferred for sampling fish eggs, spottail shiner larvae, and the following less common, but apparently demersal larvae: trout-perch Percopsis omiscomaycus, johnny darter Etheostoma nigrum, ninespine stickleback Pungitius pungitius, and slimy sculpin Cottus cognatus.     

Dispersal of fish eggs and larvae in a cascade of small hydropower plants with fish ladders

Hydrobiologia - This study was conducted to investigate fish eggs and larvae dispersal in a river stretch influenced by small hydropower plants in Southeast Brazil. The main hypothesis is...     

Fatty acid content of eggs determines antipredator performance of fish larvae

Recent work has suggested that provisioning of eggs with certain critical nutrients could be a more meaningful measure of maternal investment and correlate of offspring fitness than traditional measures of egg size. The aim of our study was to assess variability in egg quality and larva quality and to identify connections between them and the implications for larval survival. Egg size, proximate composition, and fatty acid composition were measured for 40 batches of eggs from 8 captive pairs of red drum (Osteichthyes: Sciaenops ocellatus). We reared larvae from these batches of eggs to a common size (10 mm total length, 2-3 weeks posthatching) and assessed routine activity and escape response performance of 671 individuals. Egg fatty acid composition varied more than egg size or proximate composition. Concentrations of certain long chain, highly unsaturated essential fatty acids (e.g., arachidonic acid and docosahexaenoic acid) were the only egg traits that were significantly related to larva quality (measured as escape performance). Reduced escape performance of larvae from eggs with low fatty acid concentrations was not compensated by 3 weeks of feeding on a diet enriched with fatty acids, suggesting irreversible developmental effects. Since fatty acids in eggs originate from the maternal diet, offspring survival may be determined in part by availability of nutrient-rich prey to pre-spawning adults. Migrations, regime shifts, and exploitation of marine communities could operate through this mechanism to influence recruitment in fish populations. Our findings underscore the importance of non-genetic maternal contributions to egg quality and the linkage between environmental conditions experienced by adult females and offspring fitness.