Combining Methods to Better Estimate Total Fish Richness on Temperate Reefs: The Case of a Mediterranean Coralligenous Cliff
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sampling Location
2.2. Data Collection
2.3. Data Analysis
3. Results
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Piazzi, L.; Balata, D.; Cecchi, E.; Gennaro, P.; Serena, F. Effectiveness of different investigation procedures in detecting anthropogenic impacts on coralligenous assemblages. Sci. Mar. 2014, 78, 319–328. [Google Scholar] [CrossRef] [Green Version]
- European Commission. Water Framework Directive 2000/60/EC of the European Parliament and of the Council, of 23 October 2000, Establishing a Framework for Community Action in the Field of Water Policy; Official Journal of the European Commission, 22/12/2000, L 327; European Commission: Brussels, Belgium, 2000. [Google Scholar]
- European Commission. MSFD 2008/56/EC of the European Parliament and of the Council, of 17 June 2008, Establishing a Framework for Community Action in the Field of Marine Environmental Policy (Marine Strategy Framework Directive); Official Journal of the European Commission, G.U.C.E. 25/6/2008, L 164/19; European Commission: Brussels, Belgium, 2008. [Google Scholar]
- Bracchi, V.; Savini, A.; Marchese, F.; Palamara, S.; Basso, D.; Corselli, C. Coralligenous habitat in the Mediterranean Sea: A geomorphological description from remote data. Ital. J. Geosci. 2015, 134, 32–40. [Google Scholar] [CrossRef]
- Ballesteros, E. Mediterranean coralligenous assemblages: A synthesis of present knowledge. Oceanogr. Mar. Biol. Ann. Rev. 2006, 44, 123–195. [Google Scholar]
- Piazzi, L.; Gennaro, P.; Cecchi, E.; Bianchi, C.N.; Cinti, M.F.; Gatti, G.; Guala, I.; Morri, C.; Sartoretto, F.; Serena, F.; et al. Ecological status of coralligenous assemblages: Ten years of application of the ESCA index from local to wide scale validation. Ecol. Indic. 2021, 121, 107077. [Google Scholar] [CrossRef]
- Piazzi, L. Large-scale patterns in species composition of coralligenous fish assemblages. Vie Milieu 2016, 66, 121–127. [Google Scholar]
- Piazzi, L.; Cecchi, E.; Serena, F. Spatial and temporal patterns of diversity in Mediterranean rocky reef fish assemblages. Vie Milieu 2012, 62, 129–136. [Google Scholar]
- Warnock, B.; Harvey, E.S.; Newman, S.J. Remote drifted and diver operated stereo–video systems: A comparison from tropical and temperate reef fish assemblages. J. Exp. Mar. Biol. Ecol. 2016, 478, 45–53. [Google Scholar] [CrossRef]
- Patzner, R.A. Habitat utilization and depth distribution of small cryptobenthic fishes (Blenniidae, Gobiidae, Trypyterigiidae) in Ibiza (western Mediterranean Sea). Environ. Biol. Fish. 1999, 55, 207–214. [Google Scholar] [CrossRef]
- Soldo, A.; Glavičić, I. Underwater Visual Census of Deeper Vertical Rocky Reefs. Turk. J. Fish. Aquat. Sci. 2020, 20, 785–794. [Google Scholar] [CrossRef]
- Spanier, E.; Pisanty, S.; Tom, M.; Almog-Shtayer, G. The fish assemblage on a coralligenous shallow shelf off the Mediterranean coast of northern Israel. J. Fish Biol. 1989, 35, 641–649. [Google Scholar] [CrossRef]
- Colton, M.A.; Swearer, S.E. A comparison of two survey methods: Differences between underwater visual census and baited remote underwater video. Mar. Ecol. Prog. Ser. 2010, 400, 19–36. [Google Scholar] [CrossRef] [Green Version]
- Pyle, R.L.; Earle, J.L.; Greene, B.D. Five new species of the damselfish genus Chromis (Perciformes: Labroidei: Pomacentridae) from deep coral reefs in the tropical western Pacific. Zootaxa 2007, 1671, 15–18. [Google Scholar] [CrossRef]
- Glavičić, I.; Paliska, D.; Soldo, A.; Kovačić, M. A quantitative assessment of the cryptobenthic fish assemblage at deep littoral cliffs in the Mediterranean. Sci. Mar. 2016, 80, 3–329. [Google Scholar] [CrossRef] [Green Version]
- Ackerman, J.L.; Bellwood, D.R. Reef fish assemblages: A re-evaluation using enclosed rotenone stations. Mar. Ecol. Prog. Ser. 2000, 206, 227–237. [Google Scholar] [CrossRef]
- Willis, T.J. Visual census methods underestimate density and diversity of cryptic reef fishes. J. Fish Biol. 2001, 59, 1408–1411. [Google Scholar] [CrossRef]
- Kovačić, M.; Patzner, R.A.; Schliewen, U.K. A first quantitative assessment of the ecology of cryptobenthic fishes in the Mediterranean Sea. Mar. Biol. 2012, 159, 2731–2742. [Google Scholar] [CrossRef]
- Glavičić, I.; Kovačić, M. A quantitative sampling method for assessment of deep cryptobenthic ichthyofauna using trimix diving. Acta Ichthyol. Piscat. 2016, 46, 43–47. [Google Scholar] [CrossRef] [Green Version]
- Sokal, R.R.; Rohlf, F.J. Biometry: The Principles and Practice of Statistics in Biological Research, 3rd ed.; W.H. Freeman and Co.: New York, NY, USA, 1995; p. 887. [Google Scholar]
- Froese, R.; Pauly, D. (Eds.) FishBase. World Wide Web Electronic Publication. 2021. Available online: www.fishbase.org (accessed on 15 May 2021).
- Pauly, D.; Froese, R.; Palomares, M.L.; Stergiou, K.I.; Apostolidis, C. Fish on Line. A Guide to Learning and Teaching Ichthyology using the FishBase Information System. Version 3. 2014. Available online: https://www.fishbase.se/fishonline/english/index.htm (accessed on 15 May 2021).
- Dulčić, J.; Kovačić, M. The Adriatic Sea Ichthyofauna; Split, Golden Marketing, Tehnička Knjiga i Institut za Oceanografiju i Ribarstvo: Zagreb, Croatia, 2020; p. 677. (In Croatian) [Google Scholar]
- Van der Laan, R.; Fricke, R.; Eschmeyer, W.N. (Eds.) Eschmeyer’s Catalog of Fishes: Classification. 2021. Available online: http://www.calacademy.org/scientists/catalog-of-fishes-classification/ (accessed on 12 May 2021).
- McDonald, J.H. Handbook of Biological Statistics; Sparky House Publishing: Baltimore, MD, USA, 2014; p. 296. [Google Scholar]
- Hammer, Ø.; Harper, D.A.T.; Ryan, P.D. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol. Electron. 2001, 4, 9. Available online: http://palaeo-electronica.org/2001_1/past/issue1_01.htm (accessed on 15 May 2021).
- La Mesa, G.; Molinari, A.; Gambaccini, S.; Tunesi, L. Spatial pattern of coastal fish assemblages in different habitats in North-western Mediterranean. Mar. Ecol. 2010, 32, 104–114. [Google Scholar] [CrossRef]
- Garcia-Charton, J.A.; Williams, I.; Perez-Ruzafa, A.; Milazzo, M.; Chemello, R.; Marcos, C.; Kitsos, M.-S.; Koukouras, A.; Riggio, S. Evaluating the ecological effects of Mediterranean marine protected areas: Habitat, scale and the natural variability of ecosystems. Environ. Conserv. 2000, 27, 159–178. [Google Scholar] [CrossRef]
- Sale, P.F.; Douglas, W.A. Precision and accuracy of visual census technique for fish assemblages on coral patch reefs. Environ. Biol. Fishes 1981, 6, 333–339. [Google Scholar] [CrossRef]
- Beldade, R.; Goncalves, E.J. An interference visual census technique applied to cryptobenthic fish assemblages. Vie Milieu 2007, 57, 61–65. [Google Scholar]
- Alzate, Z.F.A.; Giraldo, A. A comparison of visual and collection-based methods for assessing community structure of coral reef fishes in the Tropical Eastern Pacific. Rev. Biol. Trop. 2014, 62 (Suppl. 1), 359–371. [Google Scholar] [CrossRef] [Green Version]
- Casellato, S.; Stefanon, A. Coralligenous habitat in the northern Adriatic Sea: An Overview. Mar. Ecol. 2008, 29, 321–341. [Google Scholar] [CrossRef]
- Fasola, M.; Canova, L.; Foschi, F.; Novelli, O.; Bressan, M. Resource use by a Mediterranean rocky slope fish assemblage. Mar. Eco. 1997, 18, 51–66. [Google Scholar] [CrossRef]
Family | Method/Recorded Species | DVT and Modified DVT Visually Observed Species on Transects | SAM Recorded Species on 1 m² Squares | Species from DVT, Modified DVT, and SAM Dives Visually Noticed during Dives But Not Recorded by the Methods |
---|---|---|---|---|
Apogonidae | Apogon imberbis (Linnaeus, 1758) | + | ||
Blennidae | Microlipophrys canevae (Vinciguerra, 1880) | + | ||
Microlipophrys nigriceps (Vinciguerra, 1883) | * | |||
Parablennius incognitus (Bath, 1968) | + | |||
Parablennius rouxi (Cocco, 1833) | + | * | ||
Parablennius zvonimiri (Kolombatović, 1892) | + | |||
Carangidae | Lichia amia (Linnaeus, 1758) | (+) | ||
Seriola dumerili (Risso,1810) | (+) | |||
Trachurus trachurus (Linnaeus, 1758) | (+) | |||
Congridae | Conger conger (Linnaeus, 1758) | + | ||
Coryphaenidae | Coryphaena hippurus Linnaeus, 1758 | (+) | ||
Gadidae | Merlangius merlangus (Linnaeus, 1758) | + | ||
Gobiesocidae | Apletodon incognitus Hofrichter and Patzner, 1997 | * | ||
Lepadogaster candolii Risso, 1810 | + | |||
Gobiidae | Chromogobius zebratus (Kolombatović, 1891) | * | ||
Corcyrogobius liechtensteini (Kolombatović, 1891) | * | |||
Didogobius splechtnai Ahnelt and Patzner, 1995 | * | |||
Gammogobius steinitzi Bath, 1971 | * | |||
Gobius auratus Risso, 1810 | + | + * | ||
Gobius cruentatus Gmelin, 1789 | + | |||
Gobius fallax Sarato, 1889 | * | |||
Gobius geniporus Valenciennes, 1837 | + | |||
Gobius incognitus Kovačić and Šanda, 2016 | + | |||
Gobius kolombatovici Kovačić and Miller, 2000 | + | + * | ||
Gobius vittatus Vinciguerra, 1883 | + * | |||
Odondebuenia balearica (Pellegrin and Fage, 1907) | * | |||
Speleogobius trigloides (Zander and Jelinek, 1976) | + * | |||
Thorogobius ephippiatus (Lowe, 1839) | + | + | ||
Thorogobius macrolepis (Kolombatović, 1891) | + * | |||
Vanneaugobius dollfusi Brownell, 1978 | * | |||
Zebrus zebrus (Risso, 1827) | * | |||
Labridae | Coris julis (Linnaeus, 1758) | + | + | |
Labrus mixtus Linnaeus, 1758 | + | |||
Symphodus mediterraneus (Linnaeus, 1758) | + | |||
Symphodus melanocercus (Risso, 1810) | + | |||
Symphodus ocellatus (Linnaeus, 1758) | + | |||
Symphodus tinca (Linnaeus, 1758) | + | * | ||
Thalassoma pavo (Linnaeus, 1758) | + | |||
Lophiidae | Lophius piscatorius Linnaeus, 1758 | + | ||
Mugilidae | Chelon auratus (Risso, 1810) | (+) | ||
Oedalechilus labeo (Cuvier, 1829) | + | |||
Mullidae | Mullus surmuletus Linnaeus, 1759 | + | ||
Muraenidae | Muraena helena Linnaeus, 1758 | + | ||
Myliobatidae | Myliobatis aquila (Linnaeus, 1758) | (+) | ||
Phycidae | Phycis phycis (Linnaeus, 1766) | + | ||
Pomacentridae | Chromis chromis (Linnaeus, 1758) | + | + * | |
Scombridae | Sarda sarda (Bloch, 1793) | (+) | ||
Thunnus thynnus (Linnaeus, 1758) | (+) | |||
Scorpaenidae | Scorpaena madrensis Valeciennes, 1833 | + | ||
Scorpaena notata Rafinesque, 1810 | + | + * | ||
Scorpaena porcus Linnaeus, 1758 | + | * | ||
Scorpaena scrofa Linnaeus, 1758 | + | |||
Scyliorhinidae | Scyliorhinus stellaris (Linnaeus, 1758) | + | ||
Serranidae | Epinephelus costae (Steindachner, 1878) | + | ||
Epinephelus marginatus (Lowe, 1834) | + | |||
Serranus cabrilla (Linnaeus, 1758) | + | + | ||
Serranus hepatus (Linnaeus, 1758) | + | |||
Serranus scriba (Linnaeus, 1758) | + | + | ||
Soleidae | Synapturichthys kleinii (Risso, 1827) | + | ||
Sparidae | Boops boops (Linnaeus, 1758) | + | ||
Diplodus annularis (Linnaeus, 1758) | + | + | ||
Diplodus puntazzo (Walbaum, 1792) | + | |||
Diplodus vulgaris (Geoffroy St. Hilaire, 1817) | + | |||
Lithognathus mormyrus (Linnaeus, 1758) | + | |||
Oblada melanura (Linnaeus, 1758) | + | |||
Sarpa salpa (Linnaeus, 1758) | + | |||
Sparus aurata Linnaeus, 1758 | + | |||
Spicara flexuosa Rafinesque, 1810 | + | |||
Spicara maena (Linnaeus, 1758) | + | |||
Spicara smaris (Linnaeus, 1758) | + | |||
Spondyliosoma cantharus (Linnaeus, 1758) | + | |||
Sphyraenidae | Sphyraena sphyraena (Linnaeus, 1758) | (+) | ||
Triglidae | Chelidonichthys lastoviza (Bonnaterre, 1788) | (+) | ||
Tripterygiidae | Tripterygion delaisi Cadenat and Blanche, 1971 | + | + | |
Tripterygion melanurum Guichenot, 1850 | * | |||
Tripterygion tripteronotum (Risso, 1810) | * |
Species | DVT and Modifed DVT Frequency of Occurence (%) | Species | SAM Frequency of Occurence (%) |
---|---|---|---|
Parablennius rouxi (Cocco, 1833) | 100.00 | Corcyrogobius liechtensteini (Kolombatović, 1891) | 68.50 |
Spicara flexuosa Rafinesque, 1810 | 100.00 | Gobius auratus Risso, 1810 | 61.10 |
Spicara smaris (Linnaeus, 1758) | 100.00 | Odondebuenia balearica (Pellegrin and Fage, 1907) | 48.10 |
Gobius auratus Risso, 1810 | 100.00 | Coris julis (Linnaeus, 1758) | 27.80 |
Gobius cruentatus Gmelin, 1789 | 100.00 | Didogobius splechtnai Ahnelt and Patzner, 1995 | 20.40 |
Coris julis (Linnaeus, 1758) | 100.00 | Parablennius rouxi (Cocco, 1833) | 18.50 |
Labrus mixtus Linnaeus, 1758 | 100.00 | Chromogobius zebratus (Kolombatović, 1891) | 14.80 |
Symphodus mediterraneus (Linnaeus, 1758) | 100.00 | Chromis chromis (Linnaeus, 1758) | 14.80 |
Symphodus melanocercus (Risso, 1810) | 100.00 | Thorogobius macrolepis (Kolombatović, 1891) | 9.30 |
Symphodus tinca (Linnaeus, 1758) | 100.00 | Vanneaugobius dollfusi Brownell, 1978 | 9.30 |
Chromis chromis (Linnaeus, 1758) | 100.00 | Zebrus zebrus (Risso, 1827) | 9.30 |
Scorpaena madrensis Valeciennes, 1833 | 100.00 | Gobius vittatus Vinciguerra, 1883 | 7.40 |
Scorpaena notata Rafinesque, 1810 | 100.00 | Scorpaena notata Rafinesque, 1810 | 7.40 |
Scorpaena porcus Linnaeus, 1758 | 100.00 | Gobius kolombatovici Kovačić and Miller, 2000 | 5.60 |
Scyliorhinus stellaris (Linnaeus, 1758) | 100.00 | Thorogobius ephippiatus (Lowe, 1839) | 5.60 |
Serranus cabrilla (Linnaeus, 1758) | 100.00 | Microlipophrys nigriceps (Vinciguerra, 1883) | 3.70 |
Serranus scriba (Linnaeus, 1758) | 100.00 | Gammogobius steinitzi Bath, 1971 | 3.70 |
Boops boops (Linnaeus, 1758) | 100.00 | Speleogobius trigloides (Zander and Jelinek, 1976) | 3.70 |
Diplodus annularis (Linnaeus, 1758) | 100.00 | Serranus scriba (Linnaeus, 1758) | 3.70 |
Diplodus puntazzo (Walbaum, 1792)) | 100.00 | Diplodus annularis (Linnaeus, 1758) | 3.70 |
Diplodus vulgaris (Geoffroy St. Hilaire, 1817) | 100.00 | Apletodon incognitus Hofrichter and Patzner, 1997 | 1.90 |
Gobius fallax Sarato, 1889 | 94.44 | Gobius geniporus Valenciennes, 1837 | 1.90 |
Gobius incognitus Kovačić and Šanda, 2016 | 94.44 | Symphodus tinca (Linnaeus, 1758) | 1.90 |
Scorpaena scrofa Linnaeus, 1758 | 94.44 | Scorpaena porcus Linnaeus, 1758 | 1.90 |
Tripterygion delaisi Cadenat & Blanche, 1971 | 94.44 | Serranus cabrilla (Linnaeus, 1758) | 1.90 |
Gobius kolombatovici Kovačić and Miller, 2000 | 88.88 | Tripterygion delaisi Cadenat and Blanche, 1971 | 1.90 |
Serranus hepatus (Linnaeus, 1758) | 88.88 | Tripterygion melanurum Guichenot, 1850 | 1.90 |
Spicara maena (Linnaeus, 1758) | 66.66 | Tripterygion tripteronotum (Risso, 1810) | 1.90 |
Conger conger (Linnaeus, 1758) | 66.66 | ||
Phycis phycis (Linnaeus, 1766) | 66.66 | ||
Sarpa salpa (Linnaeus, 1758) | 61.11 | ||
Sparus aurata Linnaeus, 1758 | 61.11 | ||
Apogon imberbis (Linnaeus, 1758) | 55.55 | ||
Thorogobius ephippiatus (Lowe, 1839) | 55.55 | ||
Epinephelus marginatus (Lowe, 1834) | 55.55 | ||
Oblada melanura (Linnaeus, 1758) | 55.55 | ||
Mullus surmuletus (Linnaeus, 1758) | 50.00 | ||
Muraena helena Linnaeus, 1758 | 44.44 | ||
Epinephelus costae (Steindachner, 1878) | 44.44 | ||
Lithognathus mormyrus (Linnaeus, 1758) | 44.44 | ||
Spondyliosoma cantharus (Linnaeus, 1758) | 44.44 | ||
Merlangius merlangus (Linnaeus, 1758) | 38.88 | ||
Thalassoma pavo (Linnaeus, 1758) | 38.88 | ||
Oedalechilus labeo (Cuvier, 1829) | 16.66 | ||
Seriola dumerili (Risso,1810) | 11.11 | ||
Lophius piscatorius Linnaeus, 1758 | 11.11 | ||
Chelon auratus (Risso, 1810) | 11.11 | ||
Myliobatis aquila (Linnaeus, 1758) | 11.11 | ||
Chelidonichthys lastoviza (Bonnaterre, 1788) | 11.11 | ||
Lichia amia (Linnaeus, 1758) | 5.55 | ||
Trachurus trachurus (Linnaeus, 1758) | 5.55 | ||
Coryphaena hippurus Linnaeus, 1758 | 5.55 | ||
Sarda sarda (Bloch, 1793) | 5.55 | ||
Thunnus thynnus (Linnaeus, 1758) | 5.55 | ||
Synapturichthys kleinii (Risso, 1827) | 5.55 | ||
Sphyraena sphyraena (Linnaeus, 1758) | 5.55 |
Trait/Number of Species | DVT Recorded Species | SAM Recorded Species |
---|---|---|
(a) Maximum size | ||
Very small fish ≤ 6 cm total length (TL) | 11 | 0 |
Small fish > 6–10 cm TL | 8 | 4 |
Medium sized fish 10–50 cm TL | 9 | 32 |
Large fishes > 50 cm TL | 0 | 20 |
Fisher’s exact test p-value | <0.001 | |
(b) Relationship to the bottom | ||
Pelagic fish | 5 | 0 |
Benthopelagic species | 6 | 0 |
Hyperbenthic species | 25 | 6 |
Epibenthic species | 19 | 10 |
Cryptobenthic species | 1 | 12 |
Fisher’s exact test p-value | <0.001 | |
(c) Relationship to the reef | ||
Reef-associated species | 45 | 28 |
Occasional species | 11 | 0 |
Fisher’s exact test p-value | 0.013 | |
(d) Trophic level | ||
2–2.99 | 1 | 4 |
3–3.99 | 27 | 36 |
4–4.7 | 0 | 16 |
Fisher’s exact test p-value | <0.001 | |
(e) Catchability by commercial and recreational fishing tools | ||
Catchable | 41 | 7 |
Noncatchable | 15 | 21 |
Fisher’s exact test p-value | <0.001 | |
(f) Century of description | ||
18th century | 38 | 7 |
19th century | 15 | 13 |
20th century | 1 | 7 |
21st century | 2 | 1 |
Fisher’s exact test p-value | 0.0011 | |
(g) Taxonomy by the taxon level of orders | ||
Anguilliformes | 0 | 2 |
Blenniiformes | 5 | 2 |
Carangiformes | 0 | 6 |
Carcharhiniformes | 0 | 1 |
Gadiformes | 0 | 2 |
Gobiesociformes | 1 | 0 |
Gobiiformes | 14 | 6 |
Lophiiformes | 0 | 1 |
Mugiliformes | 0 | 2 |
Myliobatiformes | 8 | 1 |
Perciformes | 0 | 31 |
Scombriformes | 0 | 2 |
Fisher’s exact test p-value | <0.001 |
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Soldo, A.; Glavičić, I.; Kovačić, M. Combining Methods to Better Estimate Total Fish Richness on Temperate Reefs: The Case of a Mediterranean Coralligenous Cliff. J. Mar. Sci. Eng. 2021, 9, 670. https://doi.org/10.3390/jmse9060670
Soldo A, Glavičić I, Kovačić M. Combining Methods to Better Estimate Total Fish Richness on Temperate Reefs: The Case of a Mediterranean Coralligenous Cliff. Journal of Marine Science and Engineering. 2021; 9(6):670. https://doi.org/10.3390/jmse9060670
Chicago/Turabian StyleSoldo, Alen, Igor Glavičić, and Marcelo Kovačić. 2021. "Combining Methods to Better Estimate Total Fish Richness on Temperate Reefs: The Case of a Mediterranean Coralligenous Cliff" Journal of Marine Science and Engineering 9, no. 6: 670. https://doi.org/10.3390/jmse9060670