Protistan epibionts affect prey selectivity patterns and vulnerability to predation in a cyclopoid copepod

doi:10.21203/rs.3.rs-1753629/v1

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Protistan epibionts affect prey selectivity patterns and vulnerability to predation in a cyclopoid copepod

https://doi.org/10.21203/rs.3.rs-1753629/v1

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published 31 Dec, 2022

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Colonisation of crustacean zooplankton with ciliate epibionts is widespread in freshwater and marine environments. However, the ecology of such association are little studied as yet. The occurrence of ciliate epibionts on copepods and the preference towards this association with different life stages of Mesocyclops were studied from winter to spring. Relative susceptibility of zooplankton species was evaluated by analysing the epibiont colonies and zooids and relate this to the surface area of the host. The maximum epibiont infestation was recorded on copepodites followed by copepod adults rather than other zooplankton species, whereas the rotifer Asplanchna was never affected. Influence of climatic factors such as temperature on the colonisation of epibionts on basibionts was found significant. In winter (November to February) samples, copepods were infested by autotrophic epibionts whereas in late spring and early summer (March-April) heterotrophic protists (peritrichian ciliates) were the sole epibionts on copepods. We conducted experiments in the laboratory on prey selection pattern of predator by direct visual and video-graphic observations of various events (encounter, attack, capture, ingestion, prey escape) during predation by the infested and uninfested copepodites and adults of Mesocyclops.

Postencounter the attack probability was significantly lower in infested than in uninfested copepods. The present paper reports on substrate preference by epibionts and their impacts in food rich and food scarce environments. Further studied on major environmental interactions with the reproductive phenology of copepods with respect to epibionts and the cause and effect of long term association of epibionts with copepods need to be addressed.

Epibiosis

basibionts

prey selectivity

vulnerability to predation

Copepoda

Cyclopoida

Epibiosis represents the association of two organisms: the epibiont and the basibiont. The host as the basibiont accomodates the epibiont^1–2. Several commensal interactions were reported from epibiotic associations but there are also reports showing that epibionts can cause negative effects like ontogenetic or behavioural changes of the basibiont³. Fernandez-Leborans analyzed different aspects of ecological, physiological and evolutionary associations⁴. These could be opportunistic, facultative, and non-specialized, with epibionts also colonizing inert substrates, animals and plants. But it could be also an obligatory and highly specific association, with morphological and behavioural adaptations between epibiont, basibiont, and the ambient environment⁵.

Within the planktonic community, ciliated protists, certain mixotrophic flagellates and rotifers (Brachionus rubens) are frequently observed epibionts on other zooplankton^6–8. Most studies on epibiosis in planktonic communities are of systematic or structural content focussing on their spatio-temporal distribution. Very few were considering other ecological aspects^9–11. A number of ciliated protists live as epibionts on crustaceans^4,7,12,13. Furthermore, most studies tend to focus on adverse effects of epibionts on the host, such as decreased fecundity, interference with feeding, and locomotion, and increased sensitivity to contaminants^8,,13–17. Among ciliated protists, apostomatids, peritrichs, suctorians, heterotrichs, and chonotrichs are reported as epibionts on crustaceans^4,17. There are some anecdotal studies that describe the role of ciliate epibionts on hydrozoans, bryozoans, but the role of ciliates as epibionts of crustaceans has not been elucidated convincingly. In 5 major groups of crustaceans there are 30 genera of peritrichs described as epibionts¹⁷. Little is known particularly from tropical and sub-tropical ecosystems about the ecological interactions of epibionts with respect to prey predator relationships^{1, 4, 9, 15, 18}.

The association of protistian phototrophic epibionts, with the freshwater cyclopoid copepod Mesocyclops sp. are wide-spread in freshwater ecosystem, but available documents on their role in ecology, susceptibility of Mesocyclops sp. and their predation is scanty. In the present paper we attempt to solve the intriguing problem how epibionts affect basibionts in terms of feeding, mobility and being preyed upon”.

We tested the following null hypotheses: (i) Since they have a carapace and joint appendages copepods would be more susceptible to epibionts than rotifers in a natural setting; (ii) predatory copepods loaded with epibionts would require higher energy and prefer larger prey than conspecific individuals without epibionts; (iii) visual predators like planktivorous fish would selectively utilize the prey loaded with epibionts as predicted by optimal foraging models.

Environmental factors such as temperature, alkalinity, hardness, DO, pH and chlorophyll content were assessed (Table 1). Ciliate epibiont associations were observed on all rotifers, cladocerans, copepod adults and nauplii (Fig. 1) Assessment of epibiont infestation on zooplankton was carried out from 20th November 2013 to 30th April 2014. Except during the 1st week of January to the 1st week of February the different zooplankton species were observed loaded with differential numbers of epibionts (≤ 48 epibionts Ind^− 1). During this period 20–70% of zooplankton were recorded with epibionts (Fig. 1). The number of epibionts varied from species to species of the group of zooplankton as shown in Fig. 2. Association of epibionts were observed highest in copepods (Mesocyclops sp.) followed by nauplii and rotifers. Interestingly, Asplanchna was found free of epibiont infestation throughout the study period. Colonisation of epibionts were observed on Ceriodaphnia, Brachionus and Polyartha. But no ovigerous female Ceriodaphnia was observed throughout the study period. Infestation load was recorded on all stages of copepods including males, ovigerous and non-ovigerous females, copepodites, and nauplii. The species–specific frequency distribution of epibionts for zooplankton species was ≥ 5% population where one or more showed epibionts. In the present study zooplankton species loaded with epibionts were developmental stages of copepods, ovigerous copepods and other zooplankter recorded during the study such as five genera of rotifers viz. Keratella, Hexarthra, Polyarthra, Filinia, and Brachionus (Fig. 1). Infestation load of epibionts on copepod nauplii, copepod adults, Keratella cochlearis, Polyarthra vulgaris, Filinia longiseta, Brachionus rubens and Hexarthra mira are given in Fig. 2.

Table 1

Descriptive statistics of water quality parameters of wetland November 2013 to April 2014
Water quality parameters	Range	Mean ± SE
Water temperature (⁰C)	16.5–315	22.6 ± 2.25
Water depth (m)	1-1.4	1.16 ± 0.05
pH	8-8.6	8.28 ± 0.09
Dissolved Oxygen (mg/l)	5.7–6.3	6.08 ± 0.08
Chloride (mg/l)	71.2–76.5	74.13 ± 0.78
Total alkalinity (mg/l)	212–272	244 ± 10.00
Total hardness (mg/l)	252-560.5	490.5 ± 48
Chlorophyll a (µg/l)	1.53–2.37	1.78 ± 0.13
Chlorophyll b and c (µg/l)	1.24–1.96	1.71 ± 0.10

Relative susceptibility of zooplankton to epibiont infestation was highest in case of males, copepodites and non-ovigerous female cyclopoids. Ovigerous copepods were found less susceptible to epibionts (Fig. 3) than other copepod life stages.

The prevalence of epibiont numbers on ovigerous females, copepodites and nauplii was correlated with temperature (range: 16.5–31.5 ⁰C; mean ± SE: 22.6 ± 2.25). In general, 2 to 53 epibiont individuals were recorded on each individual copepod during this study. A maximum of 53 individuals of epibionts were recorded on a copepodite body on 21st November 2013. Average number of epibionts recorded per individual copepod of different developmental stages is provided in Fig. 3. Significantly lower numbers of epibionts were observed on all developmental copepod stages in February 2013 (Mann Whitney U test).

(i) Effects of epibiosis on predaton by basibionts (copepod)

Seven different types of food: Colpoda maupasi (< 120 µm) Stylonychia notophora (125 µm), Keratella cochlearis, Polyarthra vulgaris, Brachionus rubens, Asplanchna intermedia and Ceriodaphnia neonates were fed to infested and uninfested adult and copepodite stages to assess the impacts of epibiosis on basibiont predation (Fig. 4). The prey preference in copepods differed significantly between infested and uninfested adults as well as copepodites. The infested adult and copepodites prefered ciliates such as C. maupasi (Many’s α = 0.55–0.72 p < 0.01 Hotelling’sT² test) and S. notophora (Many’s α = 0.28–0.34; p < 0.01 Hotelling’s T² test) over rotifer and cladoceran prey (Fig. 4), whereas, the uninfested individuals of copepodite and adults of Mesocyclops preferred the rotifer B. rubens (Manly’s α = 0.3–0.33) followed by neonates of the cladocera C. cornuta (0.15–0.2; p < 0.05 Hotelling’s T²tes, Fig. 4).

susceptibility of Infested and uninfested cyclopoid copepods to fish predation:

The two fish species P. sarana and G. affinis showed differential selectivity pattern when fed with a combination of copepod adults and nauplii loaded with epibionts and those without epibionts. P. sarana actively selected adult copepods loaded with epibionts (Manly’s α = 0.68 ± 0.08; p < 0.001 Hotelling’s T² test), randomly ingested (Manly’s α = 0.26 ± 0.07) nauplii loaded with epibionts whereas G. affinis, showed avoidance of adult (Manly’s α = 0.06 ± 0.04) and nauplii copepods without epibionts (Fig. 5). The western mosquito fish G. affinis positively selected epibionts carrying adult copepods (Manly’s α = 0.58 ± 0.12, p < 0.01 Hotelling’sT² test) and nauplii (Manly’s α = 0.42 ± 0.11) whereas they avoided the copepods without epibionts (Fig. 5).

Nutrient rich freshwater ecosystems are frequently providing higher growth and populations of mesozooplankton (rotifers, copepods and cladocerans). However, the plankton communities are often dominated by smaller sized protozooplankton^19–20. In addition to free swimming protozooplankton, a large number of protozooplankton spends a sedentary life while exploiting resources from different parts of aquatic systems by settling on other free-swimming zooplankton¹⁷. The external body surfaces of mesozooplankton provide s substrate for epizoic protists and rotifers to settle ^{3, 8, 14, 21. 22}. Epibiosis may accrue certain ecolological aspects compared to individuals attached to non-living substrates for instance dispersal, widening their resource base²³, expansion of habitat range and protection against competitors and predators^24–25. Colonisation of ciliate epibionts are observed in various degree of association with different zooplankton taxa and their life stages. According to Bickel et al. are slightly alkaline pH values supporting favourable environments for epibionts¹⁷ and in our study the average pH was found to be 8.28 ± 0.09. Association of ciliate epibionts on invertebrates are influenced by optimal water quality parameters^4,26. In contrast, we observed no epibiont infestation on Asplanchna throughout the study period but the abundance was very low. Gilbert & Shroder and Gilbert reported that body surface chemistry of host species facilitates the prevalence of epibionts ^27–28. Cabral et al. reported for the first time ciliate epibiont infestation on different stages of copepods in the Brazilian floodplain ²⁹ but colonized naupliar stages were never observed.

The present results indicate that swimming behaviour of zooplankton is not a determinant of epibiosis rather than the external body surface is a major determinant of epibiosis. The predatory rotifer Asplanchna was never recorded with epibionts whereas even evasive zooplankton (e.g. Filinia and Polyarthra), and those showing darting swimming (cyclopoids) were observed with large numbers of epibionts. Asplanchna is an illoricate, translucent rotifer with a saccate body. The body is covered with a thin soft yellowish and proteinaceous cuticle devoid of any spines. The body morphology is changeable in shape as both internal and external organs move. Zooplankton recorded with epibionts have chitinous cuticle or carapace with spines, and appendages with relatively rough external surfaces. Our field observations support our first hypothesis that the carapace and joint appendages in copepods make this group more susceptible to epibionts under natural conditions. Several epizoans prefer to settle on rough surfaces than on smooth surfaces, and on thoracic appendages of crustaceans rather than on the carapace. Boyan et al. supported our current results emphasizing that basic requirements for attachment of peritrichs to the basibionts are as follows: the hydrophilic nature of surfaces³⁰, a suitable chemical composition and wettability, protrusion or surface texture/roughness³¹. OK

Our second hypothesis states that the predatory copepods loaded with epibionts would prefer larger prey rather than conspecific individuals without epibionts. The difference in preference between individuals which were uninfested and infested convincingly suggest the impacts of epibiosis on predation by basibionts. However the preference of uninfested copepods for larger prey (such as rotifers and cladocerans) and that in infested copepods for smaller protistan prey does not attest our second hypothesis. Probably, epibiosis restrict the swimming and darting ability of the basibionts as reported in other crustaceans^24,32. Many copepod nauplii loaded with epibionts did not moult to the copepodite stage even after two weeks of experiment and we recorded 35–48% naupliar mortality. We assume that protistan epibionts do not cause mortality directly. However, due to a large number of epibionts on the body surface nauplii become overstressed and further multiplication of protistan epibionts induce mortality. Similar observations were reported by Wu and Feng ³³.

According to a optimal foraging model the prey profitability (i.e. energy gained/energy spent in ingesting a food item) is an important determinant of prey preference^34–36. It would be in the best interest of an animal to maximize benefits, so the prey preference in an animal may switch to more beneficial food items^34,37 based on other ecological conditions (epibionts in the present case) present case³⁵. In the present case infested copepods are less mobile and unable to raptorially grasp a prey so they switch to easily capturable smaller prey. Earlier reports suggest that epibiosis provides both mimetic protection for the basibiont^4,38,39. We assume that infested copepods are less preferred prey because protistan infestation and resultant fouling activity would render the copepod less active and distasteful. Therefore, our third hypothesis speculated that the visual predators’ such as planktivorous fish would selectively utilize non-infested prey. However, in line with optimal foraging model the plantivorous ichthyoplankton preferred infested over uninfested copepods. Probably the infested copepods become more profitable prey for fish predators as the planktivorous ichthyoplankton obtain more biomass and energy content from the epibiotic protists in addition to the copepods. Therefore, epibiosis does not help copepods to escape from predators and hence becomes disadvantageous for the basibionts.

The present study has been carried out at three levels: (i) field survey to study the relative proportion of epizoic zooplankton in a natural setting; (ii) elucidation of prey selectivity patterns in copepods given a choice of co-occurring infested (by epibionts) and uninfested zooplankton, and (iii) susceptibility of infested and uninfested cyclopoid copepods to fish predation.

Field Sampling

Sampling was carried out in floodplain wetlands of the lower Gangetic basin (25⁰35′47″N 85⁰05′12″E) at Patna, India. Zooplankton samples were collected on every alternate day from November 2013 to April 2014, using a 35 µm plankton net (30 cm diameter) from the subsurface layer (50–100 cm) water at day-time. A 200-mL subsample of each net tow was preserved with modified Bouin’s fixative at a final concentration of 5%^40–41. Zooplankton was examined under a dissecting microscope and individuals with epibionts were removed from the samples and stained using the Protargol technique^{42, 43}. Identification of the ciliated protest epibionts was using the identification keys of diverse researchers ^44–49. The relative susceptibilities of zooplankton species were estimated by analyzing the epibiont colonies and zooids vs. the total zooplankton captured.

Laboratory experiments:

Experimental glass tanks were set up in quadruplicate to conduct experiment in the laboratory. Live zooplankton was collected by filtering 50 litre of water from the floodplain wetland of the River Ganga and concentrates were brought to the laboratory, and examined for the presence of epibionts. In the laboratory, 5–15 mL subsamples were examined for zooplankton species composition, ciliate epibiont prevalence (the percentage of a zooplankton group with ciliate epibionts), and epibiont load (the number of ciliate epibionts per individual zooplankter). Counts from the subsamples were extrapolated to the entire sample, and the average of the four replicates from each site was calculated. These values were used to estimate total epibiont densities (the number of epibionts per cubic meter) in the wetland. Infested (associated with epibionts) and non-infested copepods were separated under a stereozoom microscope (4X). Infested and non-infested copepods were transferred to 3-litre beakers containing 2 litres of filtered wetland water and fed with a mixture of microalgae Chlorella vulgaris, rotifers and ciliates.

Foraging experiment:

In nature changes in individual morphology, behavior and/or proximity of other organisms affect its fitness by affecting the foraging patterns of a species or its predators or of both. To elicit the impacts of epibiosis on foraging patterns of copepods and their predators we conducted two separate experiments in the laboratory: (i) epibiosis driven prey preference in copepod and (ii) vulnerability of infested and uninfested copepods to fish predation.

(i) Epibiosis drive prey preference in copepods

Prey consumption in infested and uninfested Mesocyclops aspericornis in several preliminary experiments. While designing the experiment we saught to answer: (a) what are other co-occurring prey in the natural habitat, where epibiosis on copepods were observed and (b) whether the heavy load of epibionts affect foraging patterns in the cyclopoid. To answer these questions other co-occurring species were collected from the field and acclimatized to the laboratory conditions for feeding experiment. The prey species are given in Table 1. Both infested and uninfested copepods were sufficiently pre-exposed as all the experimental organisms were simultaneously collected from the same habitat. The prey species were individually counted and introduced in equal proportions to a 400 mL crystallizing bowl, each containing one individual of Mesocyclops (either loaded by epibionts or without epibionts). Six individuals of Mesocylops were pre-starved for five hours prior to testing. The individials were used as control (infested) and treatment (uninfested). All the experimental bowls were placed in an unilluminated BOD incubator maintaining a temperature of 25 ± 1.5ᵒC and the copepods were allowed to feed for a 3h duration. Then copepods were removed and prey individuals were counted to estimate the number of consumed rotifers. For each prey type a control without food and without Mesocyclops was kept at the same density to get an estimate of multiplication during the feeding duration.

(ii) Susceptibility of infested and uninfested cyclopoid copepods to fish predation:

Two fish species, which are commonly found in the local wetlands, having high values and market demand as ornamentals, and are also recorded from the habitat where epibiosis on copepods was recorded, the mosquito fish Gambusia affinis (Baird and Girard, 1853) and Puntius sarana (Hamilton 1822). For this experiment individuals loaded with epibionts and without epibionts of nauplii and adult copepods were used as prey. Combinations of infested and uninfested individuals of adult copepods and nauplii were provided to either of the fish species in equal proportion. Three hours prior starved fish were used for the experiment and fish were allowed to feed for 60 min duration. All other protocols were same as in experiment 1. In addition, 10 individual of adult cyclopoid and nauplii each carrying epibionts were kept in separate dish to check if there was any dissociation of epibionts from the copepod during the experimental duration. Fishes were removed from the treatment dish after 60 minutes of incubation and remaining prey in each dish were counted.

Infested (associated with epibionts) and uninfested copepods were segregated under stereozoom microscope (4X). Infested and uninfested copepods were transferred in 3-litre beakers containing 2 litres of filtered wetland water and fed with a mixture of microalgae Chlorella vulgaris, rotifers and ciliates.

All experiments, including 5 replicates for each treatment, were conducted in 30 × 20 cm glass troughs containing 2 L autoclaved tap water. A series of short-term experiments was conducted to investigate the feeding rates of the mosquito fish. The initial density (Table 2) for each prey type and test duration was chosen based on preliminary feeding experiments such that at experimental termination a substantial number of prey remained unconsumed. The mosquito fish used in the experiments had sufficient exposure to all test prey species prior to testing, since they were cultured using food at different combinations of the same prey species except fish larvae. In total 32 individuals of commercially available fish, including four months old 16 individuals, each of G. affinis and P. sarana were used for the feeding trials. One individual mosquito fish was transferred from the stock aquaria to the experimental trough 6 hrs prior to the experiment and deprived of any food. After 6 h of starvation, prey was individually counted and placed gently in each experimental trough. All the experimental protocols were approved by the Research Committee of School Earth Biological and Environmental Sciences, Central University of South Bihar and the study is reported in accordance with ARRIVE guidelines (https://arriveguidelines.org), guidelines on animal experimentation.

Table 2

Length, width and dry weight of different prey species used in the feeding experiments with infested and uninfested *Mesocyclops aspericornins*. Values given are mean ± SE (n = 20).
Group	Species	Length (µm)	Width (µm)	Dry weight (µg)
Ciliophora	Colpoda maupasi	36.4 ± 4.01	18.2 ± 2.6	0.005
Ciliophora	Stylonychianotophora	88 ± 10.85	46 ± 7.3	0.008
Rotifera	Keratellacochlearis	77.8 ± 6.02	60.3 ± 7.4	0.013
	Brachionusrubens	126 ± 5.60	64.8 ± 19.8	0.16
	Polyarthra vulgaris	97.8 ± 9.58	69.3 ± 21.7	0.90
	Asplanchna intermedia	589.1 ± 26.3	302.8 ± 45.7	1.55
Cladocera	Ceriodaphnia cornuta	268 ± 9.70	152 ± 7.65	1.6

Statistical analyses

Non parametric Mann–Whitney rank tests were used to determine the differences between expected and observed values of number and dry mass ingested at particular proportions of particular prey types depending upon the two-way ANOVA results.

The difference between expected and actual prey consumption for each prey type choice test in experiment I was analyzed with repeated one-way ANOVA (for details see Kumar et al. 2012). Prey selectivity was calculated using Manly’s selectivity index (α_i)^{34, 36–37, 50} modified for a situation in which the predator consumes a substantial portion of the available prey and, hence, prey numbers in the medium decline with time, as in our experiments. The modified formula⁵¹ is

where α_i is

Manly’s α (preference index) for prey type I; n_io is the number of items of type i present at the beginning of a foraging bout; r_i is the number of items of food type i in the consumer’s diet and m is the number of prey types.

Manly’s α_i values range from 0 to 1. The α_i value for non-selective feeding is 0.143 in a multispecies (7 prey types) choice test with copepods and 0.25 in a four prey type choice test (in experiment 2) with fish. Index values above 0.143 in experiment 1 and 0.25 in experiment 2 indicate positive selection (preference) and values below indicate negative selection (avoidance). Deviations in selectivity index values from the value for non-selective feeding were tested for statistical significance using Hotelling’s T² test.

Acknowledgements

We are grateful for all staff contributing to this data set by sampling, analyzing, and providing the data. Project financially supported by Department of Environmental Science, Central University of South Bihar, Gaya. Author also would like to thank Director, ICAR-Central Inland Fisheries Research Institute for their support and guidance.

Author contributions

R. K. designed the research, analysed the zooplankton samples and water samples, planned, S. K. conducted field and laboratory work, wrote the main manuscript text and prepared Fig 1-3; A.M. revised the manuscript, analyzed the experimental zooplankton data, A. P. S. planned work, designed experiment and guided in manuscript drafting, H.U.D. Prepared graph analysis of zooplankton structure, epibionts analysis, interpreted results and prepared Figs. 4 and 5.

Additional information

The study is reported in accordance with ARRIVE guidelines (https://arriveguidelines.org). guidelines on animal experimentation.

Competing interests

The authors declare no competing interests.

Data availability statement

Data deposited in https://www.cusb.ac.in. It will be accessible after publication of manuscript

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No competing interests reported.

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Supplementary Figure 1: Zooplankton species infested with epibionts (a) Ovigerous copepod loaded with ciliates (b) adult copepod with ciliates (c) Moina (Cladocera; Crustacea) infested with algae and rotifers (Brachionus rubens) as epibionts

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Protistan epibionts affect prey selectivity patterns and vulnerability to predation in a cyclopoid copepod

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