Predator-specific inducible defenses in the rotifer Keratella tropica

1. A Patagonian strain of Keratella tropica has very different induced morphological responses to two predators – the carnivorous rotifer Asplanchna brightwelli and the interference competitor Daphnia pulex. Asplanchna induces the most exuberant morph. Compared to the basic morph, it has a fourfold longer right posterolateral spine (up to c. 115 μm), greatly elongated anterolateral and anterosubmedian spines, and no left posterolateral spine. Transitional morphs have an incompletely developed right posterolateral spine and a reduced left posterolateral spine. Daphnia induces moderate development of both posterior spines but no elongation of any anterior spines. Induction of these morphs by Asplanchna and Daphnia is mediated by kairomones. 2. The Asplanchna‐induced morph is much better defended against large (0.9 mm) Asplanchna than either the basic or Daphnia‐induced morph. The long right posterolateral spine usually prevents capture or ingestion. The Asplanchna‐ and Daphnia‐induced morphs are similarly susceptible to interference from large (3 mm) D. pulex. 3. Life‐table experiments with cohorts of the basic and Asplanchna‐induced morphs at 5 × 10³ and 2 × 10⁴ cells of Cryptomoas erosa per millilitre indicate little or no cost of the induced defense. Lifetime fecundity (13–15 offspring per female) did not differ significantly between morphs. The mean intrinsic rate of natural increase (r_m day⁻¹) of the induced morph was very slightly but significantly lower than that of the basic morph at the lower food concentration (0.46 versus 0.48) but no different from it at the higher food concentration (0.53 versus 0.54). However, spine development may involve undetermined allocation costs and environmental costs relating to interactions with other organisms. 4. It is not clear why K. tropica has separate induced responses to Asplanchna and Daphnia. Moderate spine development probably reduces damage or ingestion by small (<1.5 mm) daphniids, as in other species of Keratella, but further development may confer no protection against larger ones. Thus, the ratio of benefit to cost with daphniids (and other cladocerans) may be highest for intermediate spine development. In contrast, much greater spine development seems necessary for effective defense against Asplanchna. The more moderate response to Daphnia also may reflect less likely spatial and temporal overlap.     

Effects of an Ostracod (Cypris pubera) on the Rotifer Keratella tropica: Predation and Reduced Spine Development

This study investigates two different effects of an ostracod on a rotifer. The rotifer Keratella tropica and the ostracod Cypris pubera were cultured on the alga Cryptomonas erosa. Adult ostracods (2.2 mm body length) significantly reduced the population growth rate (r day^–1) of K. tropica from 0.42 to 0.13. Individuals of this size ingested live rotifers and produced fecal pellets with rotifer loricas. Smaller ostracods (both 0.59 and 1.61 mm body lengths) did not affect K. tropica 's population growth rate. Surprisingly, C. pubera significantly inhibited spine development in K. tropica. Rotifers cultured with juvenile, non‐predatory ostracods had similar lorica lengths but right and left posterior spines that were 10 and 30% shorter, respectively. The spine reduction induced by the ostracod kairomone is in striking contrast to the spine elongation induced in this rotifer by kairomones from copepods, cladocerans and Asplanchna. In shallow ecosystems, large ostracods that swim in the plankton may be important predators of rotifers. In addition, the presence of ostracods in plankton communities may be one of many factors affecting rotifer spine development. (© 2012 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

Cyclomorphosis in Keratella tropica (Apstein) of Lake Asejire,Nigeria

Of one thousand, one hundred and four (1104), Keratella tropica collected with a 55 m mesh plankton net from the surface of Lake Asejire from February 1974 to February 1976 lorica length and width, and the lengths of the posterior spines were measured.Lake Asejire K. tropica are among the smallest in Africa. Variations in the patterns of spine length development were independent of season as individuals without left posterior spines and with relatively long left and right posterior spines occurred as commonly in the rainy as in the dry season months.Correlations between K. tropica dimensions and thirty environmental factors underscore the importance of physical environmental factors and point to biological and genetic factors as determinants of the patterns of cyclomorphosis in K. tropica.     

Reduced investment in sex as a cost of inducible defence in Brachionus calyciflorus (Rotifera)

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Spine development in Brachionus quadridentatus from an Australian billabong: genetic variation and induction by Asplanchna

Fertilized resting eggs of Australian Brachionus quadridentatus hatched 2–3 days after hydration into females with or, more frequently, without posterior lateral spines. These females then produced clones with short-spined or long-spined phenotypes. Asplanchna girodi induced females from two short-spined clones and one long-spined clone to produce daughters with significantly longer posterior lateral spines. In all clones, there were significant differences in spine development among offspring of mothers within Asplanchna and control treatments. The range of phenotypes reported in one short-spined clone is observed in the billabong and includes much of the variation described for the species, with mehleni (long-spined) phenotypes occurring with Asplanchna. In B. quadridentatus, the ecological significance of long-spined, basic phenotypes, and of the spine-development response to Asplanchna, is unclear. In laboratory cultures, females of all clones were attached to the substratum or water surface, and were safe from Asplanchna; in nature, females are epiphytic and probably rarely susceptible to Asplanchna. Most (96%) resting eggs produced in cultures and kept under culture conditions hatched after a 7-day latent period. This raises questions regarding natural conditions which might prevent hatching and allow accumulation of resting eggs in a sediment egg bank. Hatching of resting eggs in nature may be enhanced in sediments which dry and then become flooded after rains.     

Induction and inhibition of spine development in the rotifer Keratella tropica

1. We analysed the effect of several variables on the morphology of the rotifer Keratella tropica with the aim of accounting for its morphological variability in nature. We used field data from (i) an extensive survey of Argentine lakes, (ii) a 1.5 yr, monthly sampling of Salto Grande Reservoir, and (iii) a 3-month, outdoor experiment in fish culture tanks. In addition, we performed a series of laboratory experiments aimed at isolating the effects of different variables. 2. The increase in crustacean biomass and the amelioration of their nutritional status (measured as the reciprocal of the starvation time) caused spine enlargement. In contrast, the presence of decomposers caused reduction of the spines. These results support the idea that a major proportion of the phenotypic expression of K. tropica depends on the concentration of an inducing factor, which in turn depends on the balance between release and decomposition rates of the chemical. 3. Food concentration was identified as a secondary factor affecting morphology. In agreement with records for other rotifers, food concentration and spine length were inversely related. Both factors, crustacean chemicals and food availability, seemed to act independently, at different developmental stages. Our experiments suggest, however, that the most exuberant individuals can only be induced through chemicals released by predators and competitors. 4. The presence of backswimmers (Notonectidae) resulted in individuals with very short or non-existing posterior spines. Filtrates of backswimmer-conditioned medium also produced a significant, although less striking, spine inhibition. Thus, different chemical factors seem to have opposite effects on K. tropica morphology. Those released by crustaceans induce spine elongation, while those released by backswimmers inhibit spine development. 5. Genetic differences were also identified as a source of morphological variability. Under identical laboratory conditions, different clones had spines of different length. Our experiments also suggest an inverse relationship between spine length and growth rate. The latter result, however, is based upon only three clones of K. tropica and is thus preliminary.     

Daphnia population growth but not moulting is a substantial phosphorus drain for phytoplankton

SUMMARY 1. Negative effects of zooplankton on the availability of phosphorus (P) for phytoplankton as a result of the retention of nutrients in zooplankton biomass and the sedimentation of exoskeletal remains after moulting, have been recently proposed. 2. In a mesocosm study, the relative importance of these mechanisms was tested for the freshwater cladoceran Daphnia hyalina×galeata. A total of 13 mesocosm bags was suspended in a mesotrophic German lake during summer 2000 and fertilised with inorganic P in order to obtain a total nitrogen to total P ratio closer to the Redfield ratio. D. hyalina×galeata was then added at a logarithmically scaled density gradient of up to 40 ind. L^?1. Zooplankton densities, dissolved inorganic, particulate organic (seston <100 μm), as well as total nutrient concentrations were monitored. Additionally, nutrient concentrations of sediment water removed from the bottom of the mesocosm bags via a manual pump were determined. 3. Seston carbon (C), seston P and total P were significantly negatively correlated with Daphnia densities. The amount of particulate P (～5–6 μg P L^?1) sequestered from the seston compartment by Daphnia corresponded roughly to the increase of zooplankton biomass (population growth). Soluble reactive phosphorous (SRP) was at all times high (～25–35 μg P L^?1) and possibly unavailable to phytoplankton as a result of P adsorption to calcite during a calcite precipitation event (whiting). P concentrations determined in sediment water were generally <60 μg P m^?2 and thus never exceeded 1% of the total amount of P bound in particulate matter of the overlying water column. 4. Seston C : P ratios followed a polynomial second‐order function: At Daphnia densities <40 ind. L^?1 a positive linear relationship was evident, which is explained by the stronger reduction of P compared with C in seston, and transfer of seston P to zooplankton. Highest seston C : P ratios of ～300 : 1 were observed at Daphnia densities of ～30–50 ind. L^?1, which is in agreement with proposed threshold values limiting Daphnia reproductive growth. At Daphnia densities >40–50 ind. L^?1 C : P ratios were decreased because of the strong reduction of seston C at close to constantly low seston P‐values of ～3–4 μg P L^?1. 5. At least for Daphnia, it may be concluded that – unlike population growth – the sedimentation of faecal pellets and carapaces after moulting seem negligible processes in pelagic phosphorus dynamics.     

A field and laboratory study on factors affecting polymorphism in the rotifer Keratella tropica

Summary We present data on polymorphism of the rotifer Keratella tropica from an outdoor, mesoscale experiment and a series of laboratory induction assays. In the outdoor experiment the biomass of planktonic crustaceans was noticeably depressed by larval fish predation, and associated with this depression K. tropica underwent a striking reduction of caudal spines. Subsequent laboratory studies showed that the positive association between crustacean biomass and caudal spine length was a cause and effect relationship. This is the first record of rotifer morphological change as an indirect effect of fish predation. In laboratory experiments filtrates of monospecific cultures of a cyclopoid copepod, a calanoid copepod and 5 cladocerans induced a remarkable spine development. Morphological induction showed a direct relationship with the concentration of crustaceans, both under field and laboratory conditions. Long spines were found to be strong deterrents against small predators (Acanthocyclops robustus copepodites), but were useless against large ones (females of the same species). The morphotypes of K. tropica obtained by experimental induction from a single clone encompass much of the worldwide variation of the species.     

Effect of Temperature on Fecundity,Life Span and Morphology of Long‐ and Short‐Spined Clones of Brachionus caudatus f. apsteini (Rotifera)

We investigated the effect of temperature (20, 25 and 30 °C) on fecundity, life span and morphology of the rotifer Brachionus caudatus f. apsteini. For each temperature, short posterior‐spined and long posterior‐spined clones of B. caudatus f. apsteini were individually cultured for up to six generations. The rotifers were fed Chlorella sp. at a density of 1 × 10⁶ cells ml^–1. Morphometric data (body size and spine length) were collected. Total number of offspring producing by a single female per life cycle at high temperature was higher than at low temperature. The duration of juvenile period, reproductive period, post‐reproductive period and life span of both clones of B. caudatus f. apsteini decreased with increasing temperature. All offspring of short posterior‐spined clone produce posterior spines at 20 and 25 °C, with an average length of 19.8 ± 6.6 and 11.9 ± 2.6 μm, respectively. In contrast, they cannot develop posterior spines at 30 °C, at which the average length of the posterior spine remnant was 6.4 ± 1.3 μm. On the other hand, all offspring of long posterior‐spined clone have long posterior spines with average lengths of 36.8 ± 6.1, 36.3 ± 5.2 and 36.6 ± 6.2 μm at 20, 25 and 30 °C, respectively. This study indicated that the production of posterior spines can be induced by low temperature and that short posterior‐spined and long posterior‐spined clones are genetically different. (© 2008 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

Maternal age and spine development in the rotifer Brachionus calyciflorus: increase of spine length with birth orders1

1. Maternal effects have long been known to influence phenotypic plasticity in rotifers. Females in Brachionus calyciflorus and several other species produce long‐spined offspring when the predatory rotifer Asplanchna is present; B. calyciflorus also develops short spines when food concentrations are low. These spines protect against predation and decrease food threshold concentrations. 2. Some strains of B. calyciflorus develop long spines even in the absence of Asplanchna and other environmental stimuli. We demonstrate in this study that spine length in such cases is dependent on the age of the mother. 3. In strains from Florida and Georgia, offspring spine length increased significantly with birth order, sometimes to lengths formerly observed only in the presence of Asplanchna. Significant variation in this trait was found among and within clones of a strain. Offspring body size also increased with maternal age. This is the first time maternal age has been shown to affect rotifer morphology. 4. These birth‐order effects may have important ecological implications and explain phenotypic plasticity and polymorphism in body size and spine length in populations when predators are absent and food concentrations are high. They may be a bet‐hedging mechanism to assure adaptation to rapid changes in predation pressure or food conditions.     

Direct and indirect effects of additions of chromophoric dissolved organic matter on zooplankton during large‐scale mesocosm experiments in an oligotrophic lake

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Asymmetry and variation in keratella tropica

Keratella tropica usually has two posterior spines. Both may vary in length, but the left is always shorter than the right. Sometimes the left spine is absent. Spine length varies with the length of the lorica, but there are other, external, influences. Three separate lines of evidence indicate that factors which promote spine length are related in some way to the presence of calanoid copepods.     

Cumulative effects matter: multi‐brood responses of Daphnia to hypoxia

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Elevated temperature prolongs long‐term effects of a pesticide on Daphnia spp. due to altered competition in zooplankton communities

Considerable research efforts have been made to predict the influences of climate change on species composition in biological communities. However, little is known about how changing environmental conditions and anthropogenic pollution can affect aquatic communities in combination. We investigated the influence of short warming periods on the response of a zooplankton community to the insecticide esfenvalerate at a range of environmentally realistic concentrations (0.03, 0.3 and 3 μg L^?1) in 55 outdoor pond microcosms. Warming periods increased the cumulative water temperature, but did not exceed the maximum temperature measured under ambient conditions. Under warming conditions alone the abundance of some zooplankton taxa increased selectively compared to ambient conditions. This resulted in a shift in the community composition that had not recovered by the end of the experiment, 8 weeks after the last warming period. Regarding the pesticide exposure, short‐term effects of esfenvalerate on the community structure and the sensitive taxa Daphnia spp. did not differ between the two temperature regimes. In contrast, long‐term effects of esfenvalerate on Daphnia spp., a taxon that did not benefit from elevated temperatures, were observed twice as long under warming than under ambient conditions. This resulted in long‐term effects on Daphnia spp. until 4 months after contamination at 3 μg L^?1 esfenvalerate. Under both temperature regimes, we identified strength of interspecific competition as the mechanism determining the time until recovery. However, enhanced interspecific competition under warming conditions was prolonged and explained the delayed recovery of Daphnia spp. from esfenvalerate. These results show that, for realistic prediction of the combined effects of changing environmental factors and toxicants on sensitive taxa, the impacts of stressors on the biotic interactions within the community need to be considered.     

Priority effects among young‐of‐the‐year fish: reduced growth of bluegill sunfish (Lepomis macrochirus) caused by yellow perch (Perca flavescens)?

1. When available, Daphnia spp. are often preferred by age‐0 yellow perch and bluegill sunfish because of energetic profitability. We hypothesised that predation by age‐0 yellow perch could lead to a midsummer decline (MSD) of Daphnia spp. and that priority effects may favour yellow perch because they hatch before bluegill, allowing them to capitalise on Daphnia spp. prior to bluegill emergence. 2. Data were collected from 2004 to 2010 in Pelican Lake, Nebraska, U.S.A. The lake experienced a prolonged MSD in all but 1 year (2005), generally occurring within the first 2 weeks of June except in 2008 and 2010 when it occurred at the end of June. MSD timing is not solely related to seasonal patterns of age‐0 yellow perch consumption. Nevertheless, when Daphnia spp. biomass was low during 2004 and 2006–2010 (<4 mg wet weight L^?1), predation by age‐0 yellow perch seems to have suppressed Daphnia spp. biomass (i.e. <1.0 mg wet weight L^?1). The exception was 2005 when age‐0 yellow perch were absent. 3. Growth of age‐0 bluegill was significantly faster in 2005, when Daphnia spp. were available in greater densities (>4 mg wet weight L^?1) compared with the other years (<0.2 mg wet weight L^?1). 4. We conclude that age‐0 yellow perch are capable of reducing Daphnia biomass prior to the arrival of age‐0 bluegill, ultimately slowing bluegill growth. Thus, priority effects favour age‐0 yellow perch when competing with age‐0 bluegill for Daphnia. However, these effects may be minimised if there is a shorter time between hatching of the two species, higher Daphnia spp. densities or lower age‐0 yellow perch densities.     

Similarities and differences in 13C and 15N stable isotope ratios in two non‐lethal tissue types from shovelnose sturgeon Scaphirhynchus platorynchus (Rafinesque, 1820)

We tested the hypothesis that δ¹³C and δ¹⁵N signatures of pectoral spines would provide measures of δ¹³C and δ¹⁵N similar to those obtained from fin clips for adult shovelnose sturgeon Scaphirhynchus platorynchus. Thirty‐two shovelnose sturgeon (fork length [FL] = 500–724 mm) were sampled from the lower Mississippi River, USA on 23 February 2013. Isotopic relationships between the two tissue types were analyzed using mixed model analysis of covariance. Tissue types differed significantly for both δ¹³C (P < 0.01; spine: mean = ?23.83, SD = 0.62; fin clip: mean = ?25.74, SD = 0.97) and δ¹⁵N (P = 0.01; spine: mean = 17.01, SD = 0.51; fin clip: mean = 17.19, SD = 0.62). Neither FL nor the FL × tissue type interaction had significant (P > 0.05) effects on δ¹³C. Fin clip δ¹³C values were highly variable and weakly correlated (r = 0.16, P = 0.40) with those from pectoral spines. We found a significant FL‐tissue type interaction for δ¹⁵N, reflecting increasing δ¹⁵N with FL for spines and decreasing δ¹⁵N with FL for fin clips. These results indicate that spines are not a substitute for fin clip tissue for measuring δ¹³C and δ¹⁵N for shovelnose sturgeon in the lower Mississippi River, but the two tissues have different turnover rates they may provide complementary information for assessing trophic position at different time scales.     

Growth response of cultured larvae of silver therapon Leiopotherapon plumbeus (Kner, 1864) in outdoor tanks in relation to fertilizer type and fish density

This study evaluated the effects of fertilizer type and fish density on early growth and survival of silver therapon Leiopotherapon plumbeus (Kner, 1864) larvae reared in outdoor tanks. In the first experiment, larvae (1.92 ± 0.09 mm total length) were stocked into nine, 4 m³ tanks at an initial density of 0.5 larvae L^?1 and reared for 42 days at an ambient temperature of 28.8–30.7°C. Three treatments with three replicates each were compared: organic (chicken manure, OF) or inorganic fertilizers (ammonium phosphate, IF) applied once every 2 weeks, and the unfertilized (NF) tanks serving as the control group. Water quality, zooplankton densities, survival or growth of L. plumbeus larvae did not vary significantly in either fertilized or unfertilized tanks. Fertilization resulted in elevated nutrient concentrations, which did affect survival (2.10%–6.07%) of the fish larvae. In the second experiment, larvae were stocked at densities of 0.4 or 0.6 larvae L^?1 in tanks fertilized at 4–5 days interval with OF and IF for 30 days. Growth performance of L. plumbeus larvae was affected by fish density, with significantly larger (20.04 ± 2.65 mm in total length) and higher specific growth rate (SGR; 6.97 ± 0.48% day^?1) at 0.4 larvae L^?1 than at 0.6 L^?1. Fry production did not vary significantly between fish density treatment groups given the same fertilizer types, but survival rates were improved at 0.4 L^?1. Together, production of L. plumbeus larvae in outdoor tanks can be optimized at a lower stocking density, regardless of the type of fertilizer used.     

Competition between isoetids and invading elodeids at different concentrations of aquatic carbon dioxide

1. The growth of submerged macrophytes in softwater lakes is often assumed to be carbon limited. Isoetid species are well adapted to grow at low carbon availability and therefore commonly dominate the submerged macrophyte vegetation in softwater lakes. In many such lakes, however, large‐scale invasions of fast‐growing elodeid species, replacing the isoetid vegetation, have been observed. 2. In a laboratory experiment, we tested how rising aquatic carbon availability, in interaction with different densities of the isoetid Littorella uniflora, affected the growth (and thereby the potential invasion success) of the elodeid Myriophyllum alterniflorum. For this purpose, the growth of M. alterniflorum was determined at a combination of three concentrations of dissolved CO₂ (15, 90, 200 μmol L^?1) and three densities of L. uniflora (0, 553, 1775 plants m^?2). 3. At an ambient CO₂ of 15 μmol L^?1, M. alterniflorum could not sustain itself, whereas at raised CO₂ concentrations, growth became positive and increased with higher CO₂ availability. 4. The presence of L. uniflora, independent of its density, reduced the growth of M. alterniflorum by 50%. Whether this is related to nutrient availability or other factors is not clear. 5. Despite the growth reduction of M. alterniflorum by L. uniflora, at CO₂ ≥90 μmol L^?1, L. uniflora was still overgrown by M. alterniflorum. This may imply that, in field situations, M. alterniflorum can invade softwater systems with relatively high CO₂ availability, even in the presence of dense stands of L. uniflora.     

Prey selection by Asplanchna girodi (Rotifera): the importance of prey defence mechanisms

1. Predator (laboratory-grown Asplanchna girodi and prey (several field-collected non-carnivorous rotifer species) interactions were studied in the laboratory as a function of both predator and prey densities. The clearance rates of A, girodi decreased with increasing prey density. Predator density had no effect on the feeding of A. girodi. 2. Asplanchna girodi selectively fed on Keratella cochlearis. Its clearance rates for K. cochlearis were much higher than those for Polyarthra and Brachionus. Short-spined forms (spine length less than 25 μm) showed a significantly higher susceptibility to predation than either the non-spined or the long-spined forms. 3. Large Asplanchna individuals fed selectively on reproductive females of K. cochlearis, thereby reducing the fecundity of their prey.     

Protective immunity against Leishmania major induced by Leishmania tropica infection of BALB/c mice

Leishmania (L.) tropica is a causative agent of human cutaneous and viscerotropic leishmaniasis. Immune response to L. tropica in humans and experimental animals are not well understood. We previously established that L. tropica infection induces partial protective immunity against subsequent challenge infection with Leishmania major in BALB/c mice. Aim of the present study was to study immunologic mechanisms of protective immunity induced by L. tropica infection, as a live parasite vaccine, in BALB/c mouse model. Mice were infected by L. tropica, and after establishment of the infection, they were challenged by L. major. Our findings shows that L. tropica infection resulted in protection against L. major challenge in BALB/c mice and this protective immunity is associated with: (1) a DTH response, (2) higher IFN-γ and lower IL-10 response at one week post-challenge, (3) lower percentage of CD4⁺ lymphocyte at one month post-challenge, and (4) the source of IFN-γ and IL-10 were mainly CD4⁻ lymphocyte up to one month post-challenge suggesting that CD4⁻ lymphocytes may be responsible for protection induced by L. tropica infection in the studied intervals.