The Cost for Biodiversity: Records of Ciliate–Nematode Epibiosis with the Description of Three New Suctorian Species
Abstract
:1. Introduction
2. Material and Methods
2.1. Research Areas and Sampling Strategy
2.1.1. Deep-Sea Pockmark: Madagascar Margin
2.1.2. Secca delle Fumose Shallow Vent: Gulf of Naples
2.1.3. Marine Protected Area: Gulf of Trieste
2.1.4. Mangrove Forests: French Guiana
2.1.5. Coral Reefs: Archipelago of Maldives
2.2. Samples Processing
3. Results
3.1. New Records of Associations between Nematodes and Ciliates from Deep-Sea and Shallow Water Systems
3.1.1. Deep-Sea Pockmark: Madagascar Margin
3.1.2. Secca delle Fumose Shallow Vent: Gulf of Naples
3.1.3. Marine Protected Area: Gulf of Trieste
3.1.4. Mangrove Forests: French Guiana
3.1.5. Coral Reefs: Archipelago of Maldives
3.2. Taxonomic Account of Ciliates: Systematic Position
3.3. Nematode-Ciliate Association: An Analysis
4. Discussion
4.1. Nematodes as ‘Promoters’ of Biodiversity
4.2. Advantages and Disadvantages of Nematode–Ciliate Association
4.3. The Cost for Biodiversity
4.4. Host–Epibiont Species–Specificity and the Environment
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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System Investigated | Deep-Sea Pockmark | Shallow Water HV | Nearby MPA | Mangrove Forest | Coral Reef |
---|---|---|---|---|---|
Study site | NW Madagascar margin | Gulf of Naples | Gulf of Trieste | French Guiana | Archipelago of Maldives |
Geographical area | Indian Ocean | Tyrrhenian Sea | Adriatic Sea | Atlantic Ocean | Indian Ocean |
Sampling depth | 528–775 m | 9–14 m | 18 m | 0–50 cm | 19–63 m |
Sediment tipology | Muddy | Sandy | Sandy-mud | Muddy | Sandy (in reef); silty (out reef) |
Sampling period | Sept.–Oct. 2014 | November 2017 | September 2011 | November 2017 | May 2013 |
N. of stations sampled | 2 (Site 1; Site 2) | 4 (H; G; CN and CS) | 1 (St. C1) | 3 (St. 1; St.2 and St.3) | 4 (M1, M4—in; M8, M9—out reef) |
N. of stations with infested nematodes | 1 (Site 1—inside pockmark) | 3 (G; CN and CS) | 1 (St. C1) | 2 (St. 1 and St.2) | 4 (M1; M4; M8 and M9) |
Sampling technique | MUC | Manual corer | Manual corer | Manual corer | Manual corer |
Sediment layer(s) considered | 0–1 cm | 0–1; 1–3; 3–5; 5–10 cm | 0–10 cm | 0–2; 2–10; 10–16 cm | 0–5 cm |
Sive sized used | 1 mm–32µm | 1 mm–32 µm | 1 mm–38 µm | 1 mm–32 µm | 0.5 mm–42 µm |
Extraction method | Ludox colloidal silica | Ludox colloidal silica | Ludox colloidal silica | Ludox colloidal silica | Ludox colloidal silica |
Reference | Sanchez et al. (under review) | [29] | [30] | Michelet et al. (under review) | [31] |
Study Site | Station | No. IN | B Gender | BG | ES | No. E/B | Position on the Basibiont Body |
---|---|---|---|---|---|---|---|
NW Madagascar margin-deep sea pockmark | St.1 | 15 | female (13)-male (3) | Desmodora | Paracineta homari | 1–4 | Middle body and tail region |
St.1 | 17 | female (12)-male (4) | Desmodora | Trematostoma rotunda | 1–4 | Middle body and head region | |
St.1 | 17 | female (10)-male (6) | Desmodora | Paracineta homari | 1–4 | Cloaca region | |
15% | |||||||
Gulf of Naples-shallow vent area | Site G | 25 | female (15)-male (6)-juv. (4) | Desmodora | Trematostoma rotunda | 1–8 | Along the entire body length |
Gayser | Site G | 14 | female (6)-male (5)-juv. (3) | Paradesmodora | Paracineta homari | 1–6 | Along the entire body length |
Site G | 2 | male (2) | Polysigma | Thecacineta calix | 2–5 | Along the entire body length | |
Site G | 2 | male (2) | Pseudochromadora | Paracineta homari | 1 | Tail region, before anus | |
Site G | 8 | female (4)-male (4) | Pseudodesmodora | Thecacineta calix | 2–12 | Along the entire body length | |
Site G | 2 | male (2) | Desmodoridae | Loricophrya bosporica | 1–2 | Tail region | |
Site G | 1 | female | Desmodora | Acinetopsis lynni sp. n. | 4 | Middle body and tail region | |
5% | |||||||
Gulf of Naples-shallow vent area | Site CN | 9 | female (2)-male (3)-juv. (4) | Desmodora | Trematostoma rotunda | 1–5 | Along the entire body length |
Inactive site | Site CN | 7 | female (1)-male (4)-juv. (2) | Pseudodesmodora | Thecacineta calix | 1–5 | Along the entire body length |
Site CN | 1 | male | Sygmophoranema | Thecacineta calix | 1 | Tail region | |
2% | |||||||
Gulf of Naples-shallow vent area | Site CS | 6 | female (1)-male (4)-juv. (1) | Desmodora | Paracineta homari | 1–5 | Along the entire body length |
Inactive site | Site CS | 3 | Juvenile | Paradesmodora | Paracineta homari | 1 | Middle body |
Site CS | 1 | Juvenile | Perspiria | Loricophrya susannae n. sp. | 1 | Middle body | |
Site CS | 2 | male (1)-juv. (1) | Pseudodesmodora | Thecacineta calix | 1–6 | Along the entire body length | |
Site CS | 3 | female (2)-juv. (1) | Chromaspirina | Loricophrya susannae n. sp. | 1 | Middle body | |
Site CS | 2 | male | Polysigma | Thecacineta calix | 1–2 | Along the entire body length | |
Site CS | 1 | female | Prochaetosoma | Thecacineta calix | 1 | Middle body | |
Site CS | 1 | female | Perepsilonema | Thecacineta fumosae n. sp. | 1 | Middle body | |
2% | |||||||
Gulf of Trieste | St. C1 | 1 | juvenile | Pseudochromadora | phoronts of Apostomatia | 19 | Along the entire body length |
0.2% | |||||||
French Guiana-Mangrove forest | St. 1 | 4 | male (1)-female (3) | Desmodora | Paracineta homari | 5–6 | Along the entire body length |
Polluted area | St. 1 | 2 | female | Desmoscolex | Loricophrya bosporica | 1 | Tail region |
0.5% | |||||||
French Guiana-Mangrove forest | St. 2 | 15 | male | Desmodora | Loricophrya bosporica | 6 | Along the entire body length |
Medium polluted area | St. 2 | 1 | female | Spirinia | Cothurnia sp. | 2 | Tail region |
2.7% | |||||||
Archipelago of Maldives - coral reef | M1 | 1 | male | Paradesmodora | Loricophrya sivertseni and L. stresemanni | 2 | After cloaca opening |
Inner reef | M4 | 1 | female | Croconema | Thecacineta calix | 5 | Intestine region and caudal region before anus |
M4 | 1 | male | Paradesmodora | Thecacineta cothurnioides | 1 | Second half of the body, before cloaca | |
1% | |||||||
Outer reef | M8 | 1 | juvenile | Desmodorella | Paracineta sp. | 1 | First half of pharingeal region |
M9 | 1 | female | Echinodesmodora | Thecacineta cothurnioides | 1 | Second half of intestine region | |
1% |
(A) Epibiont Effects on Basibiont | |
Cost | Benefit |
Change of properties of basibiont surface | Epibiont mechanisms against predators |
into basibiont–epibiont–water interface | that can serve concurrently for the basibiont |
Increase friction with the water = decrease | Associational resistance |
basibiont velocity | |
Increase predation risk by modifying chemical signals | Camouflage |
and by increasing the basibiont weight = motility | Nutrient flow from epibiont and vitamins |
reduction | |
Decrease the visus of the basibiont and cause | Ciliate epibionts adhere to external cuticular |
wounds on the cuticle | layer of the basibiont with no effect and without |
causing any arm = neutral effect | |
A high infestation makes difficult for the host | |
to maintain the position into the water and sediment | |
Harmful energetic cost especially when energy | |
conditions are limited | |
Decreased reproduction, growth and survivorship: | |
epibiont can be a hindrance to mating | |
Starvation for food competition with epibiont | |
in the case of sharing of feeding source(s) | |
Increase basibiont vulnerability to infections | |
and energy cost for locomotion | |
Diminish gas exchanges if they colonize | |
gas exchange surface | |
Epibionts as cause for stress on basibiont by | |
compromising the capacity of defense and competition | |
(B) Basibiont Effects on Epibiont | |
Cost | Benefit |
Exposure to inadequate environmental conditions | Available surface to colonize on which to live |
Removing of epibiont by abrasion or by moult | Shock-absorbing substratum |
Capture of the basibiont by predator | Dispersion of epibiont mobile life stage and gene |
flow | |
Competition with other ciliates attached to the same | Free transport for the epibiont |
basibiont or with conspecific when abundant | |
Shared doom with basibiont | Protection against predators |
Exposure to detrimental host defense | Favorable hydrodynamic conditions |
Increasing in availability of nutrients for the epibiont |
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Baldrighi, E.; Dovgal, I.; Zeppilli, D.; Abibulaeva, A.; Michelet, C.; Michaud, E.; Franzo, A.; Grassi, E.; Cesaroni, L.; Guidi, L.; et al. The Cost for Biodiversity: Records of Ciliate–Nematode Epibiosis with the Description of Three New Suctorian Species. Diversity 2020, 12, 224. https://doi.org/10.3390/d12060224
Baldrighi E, Dovgal I, Zeppilli D, Abibulaeva A, Michelet C, Michaud E, Franzo A, Grassi E, Cesaroni L, Guidi L, et al. The Cost for Biodiversity: Records of Ciliate–Nematode Epibiosis with the Description of Three New Suctorian Species. Diversity. 2020; 12(6):224. https://doi.org/10.3390/d12060224
Chicago/Turabian StyleBaldrighi, Elisa, Igor Dovgal, Daniela Zeppilli, Alie Abibulaeva, Claire Michelet, Emma Michaud, Annalisa Franzo, Eleonora Grassi, Lucia Cesaroni, Loretta Guidi, and et al. 2020. "The Cost for Biodiversity: Records of Ciliate–Nematode Epibiosis with the Description of Three New Suctorian Species" Diversity 12, no. 6: 224. https://doi.org/10.3390/d12060224