Context‐dependent outcomes in a reproductive mutualism between two freshwater fish species

1. The development of encompassing general models of ecology is precluded by underrepresentation of certain taxa and systems. Models predicting context‐dependent outcomes of biotic interactions have been tested using plants and bacteria, but their applicability to higher taxa is largely unknown.
2. We examined context dependency in a reproductive mutualism between two stream fish species: mound nest‐building bluehead chub Nocomis leptocephalus and mountain redbelly dace Chrosomus oreas, which often uses N. leptocephalus nests for spawning. We hypothesized that increased predator density and decreased substrate availability would increase the propensity of C. oreas to associate with N. leptocephalus and decrease reproductive success of both species.
3. In a large‐scale in situ experiment, we manipulated egg predator density and presence of both symbionts (biotic context), and replicated the experiment in habitats containing high‐ and low‐quality spawning substrate (abiotic context).
4. Contradictory to our first hypothesis, we observed that C. oreas did not spawn without its host. The interaction outcome switched from commensalistic to mutualistic with changing abiotic and biotic contexts, although the net outcome was mutualistic.
5. The results of this study yielded novel insight into how context dependency operates in vertebrate mutualisms. Although the dilution effect provided by C. oreas positively influenced reproductive success of N. leptocephalus, it was not enough to overcome both egg predation and poor spawning habitat quality. Outcomes of the interaction may be ultimately determined by associate density. Studies of context dependency in vertebrate systems require detailed knowledge of species life‐history traits.

     

The Life Cycle of Trypanoplasma bullocki (Zoomastigophorea: Kinetoplastida)1

The leech Calliobdella vivida (Verrill) is the vector of Trypanoplasma bullocki. At 10°C, infective-stage flagellates were first present in the leech's proboscis sheath five days after feeding. At 5°C, infective-stage flagellates were not present in the leech's proboscis sheath until 10 days after feeding, but at 20°C, flagellates were located there as early as 24 h after feeding. Infected leeches retained flagellates through three subsequent feeds on uninfected fish. When flagellates were first observed in hogchoker, Trinectes maculatus (Bloch & Schneider), they were much larger than infective stages from the leech. Average flagellate length then decreased during early acute phase, but gradually increased thereafter. Peak parasitemia was greater in a hogchoker inoculated by only one leech but held at colder temperature than in a hogchoker inoculated by 45 leeches, suggesting that temperature may be more important than inoculum in determining peak parasitemia. Cell division in the fish host is described. SEM studies of fish blood flagellates revealed a pre-oral ridge and a cytostome.     

Does body size difference in the leeches Glossiphonia complanata (L.) and Helobdella stagnalis (L.) contribute to co-existence?

The effect of predator and prey body size on the feeding success of the British lake-dwelling leeches Glossiphonia complanata and Helobdella stagnalis was examined in the laboratory, and any involvement of size difference between the leeches in allowing coexistence in the field assessed. G. complanata breeds in advance of H. stagnalis and maintains a body size advantage throughout their annual life-cycle. In experiments, conducted at 14 °C and a photoperiod of 16 hrs L: 8 hrs D, three size classes of leeches of each species were each exposed to each of three size classes of each of five prey species, viz. Tubifex sp., Chironomus sp., Asellus aquaticus, Lymnaea peregra and Potamopyrgus jenkinsi. For each prey species, three different types of experiments were performed: one leech exposed to four prey individuals; four leeches of the same species with sixteen prey; and two leeches of each species with sixteen prey. In the first experiment, all sizes of G. complanata were capable of feeding on all sizes of the prey types offered; the same was true for H. stagnalis with exceptions of feeding on large A. aquaticus and large L. peregra. For both species, but especially for G. complanata, there was a trend within each size class of leech for decreasing proportions of fed leeches with increasing prey size, and within each size class of prey for an increasing proportion of fed leeches with increasing leech size; however there were several exceptions to these trends. Both leeches fed extensively on Tubifex sp. but there were significant differences in the proportions feeding on other prey types; G. complanata fed more on A. aquaticus and the two snail species, and less on Chironomus, than H. stagnalis. The effect of increasing the number of leech individuals from one to four individuals, of the same or mixed species, had little effect on the proportion of leeches which had fed. It is concluded that large G. complanata will have access to large individuals of certain prey taxa denied H. stagnalis, which may lessen the intensity of interspecific competition.     

Correlates of elemental‐isotopic composition of stream fishes: the importance of land‐use,species identity and body size

The isotopic (δ¹³C and δ¹⁵N) and stoichiometric (C:N:P) compositions of four fish species (Family Centrarchidae: Lepomis auritus, Lepomis cyanellus; Family Cyprinidae: Nocomis leptocephalus, Semotilus atromaculatus) were examined across four North Carolina Piedmont streams arrayed along an urbanization gradient. Both isotopic and stoichiometric composition of fishes appeared to track changes occurring in basal resource availability. Values of δ¹³C of basal resources and consumers were more enriched at the most urbanized streams. Similarly, basal resources and consumers were δ¹⁵N–enriched at more urbanized streams. Basal resource stoichiometry varied across streams, with periphyton being the most variable. Primary consumers stoichiometry also differed across streams. Intraspecific variation in fish stoichiometry correlated with the degree of urbanization, as the two cyprinids had higher N content and L. cyanellus had higher P content in more urbanized streams, probably due to enrichment of basal resources. Intrinsic factors, specifically species identity and body size also affected stoichiometric variation. Phosphorus (P) content increased significantly with body size in centrarchids, but not in cyprinids. These results suggest that although species identity and body size are important predictors of elemental stoichiometry, the complex nature of altered urban streams may yield imbalances in the elemental composition of consumers via their food resources.     

Mutualism or parasitism: Partner abundance affects host fitness in a fish reproductive interaction

相似文献   

Competitive interactions between the lake-dwelling leeches Glossiphonia complanata and Helobdella stagnalis: an experimental investigation of the significance of a food refuge

The glossiphoniid leeches Helobdella stagnalis and Glossiphonia complanata co-exist on the stony shores of British lakes. Because both species have a similar life-style and are food limited, the question arises as to how coexistence persists. Laboratory experiments investigated if either leech has a competitive advantage on three foods, viz. oligochaete worms (Tubifex sp.), snails (Lymnaea peregra), and a worm-plus-snail mixture. A variety of densities with a range of ratios of the two leeches, and monospecific controls were used. The level of feeding ensured increasing food shortage with rising leech density. Experiments, conducted at 14° C, lasted 3 months. Regression values for growth against density in the controls indicated the occurrence of intraspecific competition in both leech species. Light mortality occurred at the highest densities. G. complanata gained significantly less weight in mixed leech cultures than in monospecific cultures at some of the highest densities when fed worms, but more weight when fed on snails. The opposite was true for H. stagnalis. When both prey types were provided, no differences at any density were observed for either leech. Differences in bodysize and feeding strategy between the leeches may be implicated in determining their feeding success on the prey types. Because the anti-predatory responses (e.g. shaking) exhibited by L. peregra are less when encountering an inactive than an active leech, the sit-and-wait strategy of G. complanata may aid snail capture. In contrast, the seek-out strategy of H. stagnalis, coupled with its relatively smaller size, may result in fewer successful captures. The active hunting strategy of H. stagnalis may be advantageous for the capture of oligochaetes which are relatively less mobile than snails. Offering both prey types simultaneously would have had an ameliorating influence on interactions between the two leeches. Findings provide support for the hypothesis that long-term co-existence between the two glossiphoniids in British lakes may depend, in part at least, on the occurrence of a snail food refuge for G. complanata.     

Study on foraging mechanism of leeches with different feeding habits based on chemoreception and foraging behavior

The leeches Whitmania pigra and Hirudo nipponia live in similar environments but have different feeding habits. At present, there are few studies of the foraging mechanism of leeches with different feeding habits. In this study, we first used maze tests to show that these two species of leeches could locate and distinguish their prey through chemosensory activity without mechanical stimulation. However, the two leech species have different foraging behaviors: Individuals of W. pigra move slowly and repeatedly adjust direction through probing and crawling to detect the location of prey (snails), whereas individuals of H. nipponia move quickly, and after determining the location of food (porcine blood), they quickly swim or crawl to the vicinity of their prey. Scanning electron microscopy (SEM) revealed that there are two types of sensory cilia and pore structures related to mucus secretion in the heads of both leeches. There are two differently sized types of chemoreceptors on the dorsal lip in W. pigra, which may have different functions during foraging, whereas in H. nipponia there is only one type of chemoreceptor, which is small. We detected the chemical components in the natural food of these two leech species by UHPLC–MS. There were 934 metabolites in the body fluid of snails and 751 metabolites in porcine serum; five metabolites unique to the body fluid of snails and to porcine serum were screened as candidate feeding attractants. Of these metabolites, betaine and arginine effectively attracted individuals of W. pigra and H. nipponia, respectively. In summary, leeches with different feeding habits use chemoreceptors to sense external chemical signals when foraging, and there are significant differences between species in foraging behavior, chemoreceptors, and attractants.     

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.     

Fish-egg predation by the small clingfish <Emphasis Type="Italic">Pherallodichthys meshimaensis</Emphasis>(Gobiesocidae) on the shallow reefs of Kuchierabu-jima Island,southern Japan

Synopsis We observed predation of demersal fish eggs by the clingfish Pherallodichthys meshimaensis on the shallow reefs of Kuchierabu-jima Island, southern Japan. The processes of egg predation varied with the target species. For targeting of eggs of the combtooth blenny Istiblennius edentulus, up to 65 individuals of the clingfish gathered around the I. edentulus nest hole. Some individuals succeeded in intruding into the hole and fed on eggs while the egg-guarding male of I. edentulus temporarily left the nest. For targeting of eggs of the triplefin blenny Helcogramma obtusirostris, solitary clingfish individuals closely approached spawning females of H. obtusirostris at nests on open surfaces of rocks. Most clingfish contained only fish eggs in their diets, and these fish-egg eaters had larger body sizes than individuals that mainly fed on harpacticoid crustacea. Thus, P. meshimaensis may change its feeding habits when growing to an obligate fish-egg eater targeting demersal egg spawners.     

The Natural Feeding and Resource Partitioning of Erpobdella octoculata L. and Erpobdella testacea SAV. in Lake Esrom,Denmark

The natural feeding and competitive interactions between populations of Erpobdella ostoculata and Erpobdella testacea were investigated in Lake Esrom, Denmark, during 1979/80. Statistical analysis revealed that the size of the leeches was the main factor involved in resource utilization. Size-specific feeding included differences in the numerical composition of diets and the size of individual prey. Five weight classes of Erpobdella spp. were distinguished. The number of prey per leech increased from 1.63-2.84 for the first to the fifth weight class, whereas diversity in feeding averaged 1.71 prey per leech. Quantification of competitive interactions indicated that the temporal differences in weight class composition of the two species were sufficient to explain coexistence, although both species have an annual life cycle, and neither species showed taxonomic food refuges.     

Life Cycle and Feeding Habits of Dina punctata Johansson, 1927 (Erpobdellidae,Hirudinea) in a Small Carpathian Stream

The leech Dina punctata Johanson, 1927 inhabits various types of running waters. This species appeared in Slovakia probably after the first Rhine‐Main‐Danube canal was built. Because little is known about its ecology, the aim of our study was to analyze the life cycle, individual growth rate, reproduction parameters and food composition of D. punctata in the Vydrica Stream. Samples of leeches were taken mainly each month from April 2003 to November 2004. The leech D. punctata had maximal 2‐year life cycle there. Mature leeches, which were recognized by the presence of clitella, were present from April to the end of August. The most individuals mature at the age of 1 year. The breeding season of D. punctata peaks in June. The number of eggs per one cocoon is from 3 to 12. The mean successfulness of development of egg to embryo is 58%. Larvae from the family Chironomidae (28%), Gammarus fossarum (20%) and oligochaetes from the subfamily Naidinae (17%) are the dominant components of the feeding niche. (© 2011 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

The Feeding Strategies of the Leech Erpobdella octoculata (L.): A Laboratory Study

The feeding behaviour of the freshwater leech Erpobdella octoculata was analysed by exposing potential invertebrate and vertebrate prey organisms (alive, wounded or dead) to leech attack in dishes, in the laboratory. The fact that E. octoculata is a macrophagous feeder that swallows living prey organisms whole (preferentially Chironomus larvae) is documented. However, it was repeatedly observed that adult leeches sucked the body fluids from wounded larvae. Likewise, cut pieces of earthworms, dead crustaceans and crushed water snails were attacked and the soft parts sucked in with the aid of the unarmed pharynx. Adult leeches sucked the body fluids from dead, decaying bodies of vertebrates (fish, newt larvae). Newly hatched young are blood suckers that rapidly attacked the wounded regions of Chironomus larvae and other invertebrates such as crushed water snails. It is concluded that the common leech E. octoculata is not only a predator, but also a fluid sucker and a scavenger. The ecological implications of this finding are discussed.     

Interspecific nesting in marine fishes: spawning of the spinynose sculpin, <Emphasis Type="Italic">Asemichthys taylori</Emphasis>, on the eggs of the buffalo sculpin, <Emphasis Type="Italic">Enophrys bison</Emphasis>

Subtidal spawning of the cottid fish Enophrys bison occurs in southern British Columbia, where in the field a smaller subtidal cottid, Asemichthys taylori, exclusively utilizes E. bison nests by overlaying its own eggs on top of the E. bison eggs. In the laboratory, spawning of A. taylori in the absence of E. bison nests was observed to occur adjacent to eggs of another sculpin, Icelinus borealis, but no spawning of A. taylori was observed in the field in association with nests of any fish other than E. bison. The E. bison male guards the composite cluster of egg masses, and the A. taylori eggs hatch faster than the earlier laid E. bison eggs. Enophrys bison embryonic development appears retarded by overlying A. taylori eggs so the spawning by A. taylori on E. bison egg masses is a form of nesting parasitism, a behavior previously unknown among marine fishes. This study is the first report of interspecific nesting for marine fishes.     

Using metabarcoding to compare the suitability of two blood‐feeding leech species for sampling mammalian diversity in North Borneo

The application of high‐throughput sequencing (HTS) for metabarcoding of mixed samples offers new opportunities in conservation biology. Recently, the successful detection of prey DNA from the guts of leeches has raised the possibility that these, and other blood‐feeding invertebrates, might serve as useful samplers of mammals. Yet little is known about whether sympatric leech species differ in their feeding preferences, and whether this has a bearing on their relative suitability for monitoring local mammalian diversity. To address these questions, we collected spatially matched samples of two congeneric leech species Haemadipsa picta and Haemadipsa sumatrana from lowland rainforest in Borneo. For each species, we pooled ~500 leeches into batches of 10 individuals, performed PCR to target a section of the mammalian 16S rRNA locus and undertook sequencing of amplicon libraries using an Illumina MiSeq. In total, we identified sequences from 14 mammalian genera, spanning nine families and five orders. We found greater numbers of detections, and higher diversity of OTUs, in H. picta compared with H. sumatrana, with rodents only present in the former leech species. However, comparison of samples from across the landscape revealed no significant difference in mammal community composition between the leech species. We therefore suggest that H. picta is the more suitable iDNA sampler in this degraded Bornean forest. We conclude that the choice of invertebrate sampler can influence the detectability of different mammal groups and that this should be accounted for when designing iDNA studies.     

Impact of drought upon fish assemblage structure in two South Carolina Piedmont streams

The effects of drought on fish assemblages were studied in the Indian Creek (228 km²) and Kings Creek (46 km²) watersheds located in the Piedmont Province of South Carolina. Water and fish samples were collected at 13 localities during drought conditions in 2000 and again under post-drought conditions in 2003. Abundance, species richness, and Simpson’s diversity were calculated for each locality, and the masses and lengths of individual fishes were measured to determine total biomass and length distributions for each species. Assemblages were significantly different from 2000 to 2003 at 10 of the 13 sample localities (χ² test for association; p < 0.05). The family Cyprinidae (minnows) was numerically dominant in both years and in both watersheds, but their dominance declined somewhat following the drought due to lower numbers of Nocomis leptocephalus and Notropis lutipinnis in 2003 collections. However, some cyprinids increased in abundance in 2003 collections, most notably Semotilus atromaculatus and Hybopsis hypsinotus. Abundance of catostomids (suckers) and ictalurids (catfish) was also decreased post drought. Conversely, centrarchids (sunfish) increased in dominance in 2003, especially the species Lepomis macrochirus and Lepomis gulosus. Many more juveniles and young of the year were observed in 2003 collections, suggesting that most species exhibited greater reproductive success following the drought. The significant differences in water chemistry observed between the two years were not associated with any change in fish community structure. Instead, we attributed the observed differences in fish assemblages to changes in habitat structure associated with higher rainfall during post-drought conditions. Finally, sample localities showed high variability in common measures of assemblage structure, including abundance, species richness, and diversity. We hypothesize that the observed variability in community structure is caused by the heterogeneous habitat structure and morphology of these small Piedmont Province streams.     

Communal Spawning in the Common Frog Rana temporaria– Egg Temperature and Predation Consequences

Females of the common frog, Rana temporaria, spawn synchronously at communal breeding sites, forming a communal egg mass of individual spawn clumps. A total of four spawning sites were studied. In the centre of the communal egg mass, daily maximum temperature was higher and minimum temperature lower than further out. Spawn clumps in the centre of the communal egg mass developed faster than single spawn clumps. In the centre of the egg masses, some spawn clumps suffered almost total egg mortality. This was probably the consequence of a cold spell with sub‐zero temperatures in combination with a tendency for low minimum temperatures in the centre. In a laboratory study, worm leeches, Erpobdella spp., fed readily on eggs of common frog, while horse leeches, Haemopis sanguisuga, hardly ate any eggs. At the spawning sites, most worm leeches were found in single spawn clumps, far from the communal egg mass. Females which spawned late, when most of the spawning was over, preferred to spawn in the centre of the communal egg mass. This suggests that there is a net advantage for eggs in spawn clumps laid in the centre.     

Genetic barcoding of marine leeches (Ozobranchus spp.) from Florida sea turtles and their divergence in host specificity

Ozobranchus margoi and Ozobranchus branchiatus are the only two species of marine turtle leeches (Ozobranchus spp.) known to inhabit the Atlantic coast of the United States and the Gulf of Mexico. In early reports of fibropapillomatosis (FP) in green turtles (Chelonia mydas), O. branchiatus was implicated as a vector in the transmission of Fibropapilloma‐associated turtle herpesvirus (FPTHV). It is imperative that the leech species be identified to elucidate the role Ozobranchus spp. may play in disease transmission. In this study, Ozobranchus branchiatus has been identified for the first time on a loggerhead (Caretta caretta) turtle, and the molecular data for this species is now available for the first time in GenBank. Both species of leeches were also found infecting a single C. mydas. Using morphological taxonomy combined with distance‐ and character‐based genetic sequence analyses, this study has established a DNA barcode for both species of Ozobranchus spp. leech and has shown it can be applied successfully to the identification of leeches at earlier stages of development when morphological taxonomy cannot be employed. The results suggest a different haplotype may exist for O. branchiatus leeches found on C. caretta versus C. mydas. Leech cocoon residue collected from a C. mydas was identified using the new method.     

Consumption of coral propagules represents a significant trophic link between corals and reef fish

Mass spawning of corals provides a large seasonal pulse of high-energy prey that potentially benefits reef fish that are capable of capturing and digesting coral propagules. This study examines the range of fish species that consume coral propagules and also tests whether reef fish experience a significant increase in physiological condition when feeding on coral propagules. Thirty-six species of diurnal reef fish were seen to consume coral propagules released during mass coral spawning. Stomach content analyses of three reef fish species (Pomacentrus moluccensis, Abudefduf whitleyi, and Caesio cunning) revealed that both P. moluccensis and A. whitleyi feed almost exclusively on coral propagules during mass coral spawning. Fish feeding extensively on coral propagules also amassed considerable lipid stores, which could greatly improve the quality and survivorship of their progeny. In contrast, C. cunning consumed only very small quantities of coral propagules, and showed no detectable change in lipid stores during the course of the study. This study provides the first direct evidence that reef fish benefit from mass coral spawning, and reveals a potentially significant trophic link between scleractinian corals and reef fish. Accepted: 9 June 2000     

Egg shape mimicry in parasitic cuckoos

Parasitic cuckoos lay their eggs in nests of host species. Rejection of cuckoo eggs by hosts has led to the evolution of egg mimicry by cuckoos, whereby their eggs mimic the colour and pattern of their host eggs to avoid egg recognition and rejection. There is also evidence of mimicry in egg size in some cuckoo–host systems, but currently it is unknown whether cuckoos can also mimic the egg shape of their hosts. In this study, we test whether there is evidence of mimicry in egg form (shape and size) in three species of Australian cuckoos: the fan‐tailed cuckoo Cacomantis flabelliformis, which exploits dome nesting hosts, the brush cuckoo Cacomantis variolosus, which exploits both dome and cup nesting hosts, and the pallid cuckoo Cuculus pallidus, which exploits cup nesting hosts. We found evidence of size mimicry and, for the first time, evidence of egg shape mimicry in two Australian cuckoo species (pallid cuckoo and brush cuckoo). Moreover, cuckoo–host egg similarity was higher for hosts with open nests than for hosts with closed nests. This finding fits well with theory, as it has been suggested that hosts with closed nests have more difficulty recognizing parasitic eggs than open nests, have lower rejection rates and thus exert lower selection for mimicry in cuckoos. This is the first evidence of mimicry in egg shape in a cuckoo–host system, suggesting that mimicry at different levels (size, shape, colour pattern) is evolving in concert. We also confirm the existence of egg size mimicry in cuckoo–host systems.     

Aspects of the biology of the catfish Clarias lazera (Cuv. & Val.) related to its economic cultivation

The seasonal abundance, population structure, reproduction, feeding, respiratory adaptations and tolerance were studied in the catfish Clarias lazera (Cuv. & Val.) in the reservoir of Jebel Aulia on the White Nile, and in the Green-Belt canals near Khartoum. Continuous monitoring of the ripe, spent and spawning females and immature fish in the population revealed that C. lazera breed synchronously in the autumn in the reservoir and rather sporadically in the canals. Medium-sized females were more fecund than old and young females. Administration of pituitary extract enhanced maturation, induced spawning in mature fish, stimulated body growth, especially in maturing specimens, and produced, as a side-effect, a diuretic response. Mature fish depended on pulmonary respiration for about 45% of the total oxygen requirement. C. lazera fed preferentially on its fry and on decayed proteinaceous food. The suitability of this species for economic cultivation is discussed.