Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Demographic modelling of giant sea anemones: population stability and effects of mutualistic anemonefish in the Jordanian Red Sea

Austin K. Dixon A , Matthew J. McVay B and Nanette E. Chadwick B C
+ Author Affiliations
- Author Affiliations

A Department of Desert Ecology, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, 8499000, Israel.

B Department of Biological Sciences, 101 Rouse Life Sciences Building, Auburn University, Auburn, AL 36849, USA.

C Corresponding author. Email: chadwick@auburn.edu

Marine and Freshwater Research 68(11) 2145-2155 https://doi.org/10.1071/MF16361
Submitted: 26 October 2016  Accepted: 5 April 2017   Published: 20 June 2017

Abstract

Giant sea anemones serve as important hosts for mutualistic anemonefish on Indo-Pacific coral reefs, but their population dynamics and turnover rates remain largely unknown. We used size-based demographic models to determine recruitment, changes in body size and mortality of bulb-tentacle anemones Entacmaea quadricolor and leathery anemones Heteractis crispa over 2 years on coral reefs in the northern Red Sea, Jordan. Individuals recruited at consistent rates and grew rapidly until they reached ~300-cm2 tentacle crown surface area, then mostly remained static or shrank. Mortality rate decreased with body size, and the retention of large individuals strongly influenced population size. Individuals of H. crispa were more dynamic than those of E. quadricolor, possibly due to their hosting significantly smaller anemonefish. Both populations were abundant and stable but dynamic in terms of individuals, with estimated turnover times of only ~5 and 3 years for E. quadricolor and H. crispa respectively. We conclude that some giant anemones may be short lived relative to their fish symbionts, and that stasis rates of large individuals disproportionately affect their populations. These results have implications for conservation management strategies of these major cnidarians on coral reefs, and indicate wide variation between species in the population-level effects of mutualistic interactions.

Additional keywords: coral reef, mutualism, population dynamics, recruitment, symbiosis.


References

Abu-Hilal, A., and Al-Najjar, T. (2009). Marine litter in coral reef areas along the Jordan Gulf of Aqaba, Red Sea. Journal of Environmental Management 90, 1043–1049.
Marine litter in coral reef areas along the Jordan Gulf of Aqaba, Red Sea.Crossref | GoogleScholarGoogle Scholar |

Allen, G. R., Kaufman, L., and Drew, J. A. (2008). Amphiprion barberi, a new species of anemonefish (Pomacentridae) from Fiji, Tonga, and Samoa. Aqua – Journal of Ichthyology and Aquatic Biology 14, 105–114.

Allen, G. R., Drew, J., and Fenner, D. (2010). Amphiprion pacificus, a new species of anemonefish (Pomacentridae) from Fiji, Tonga, Samoa, and Wallis Island. Aqua International Journal of Ichthyology 16, 129–138.

Babcock, R. C. (1991). Comparative demography of three species of scleractinian corals using age- and size-dependent classifications. Ecological Monographs 61, 225–244.
Comparative demography of three species of scleractinian corals using age- and size-dependent classifications.Crossref | GoogleScholarGoogle Scholar |

Batchelder, H. P., and Gonor, J. J. (1981). Population characteristics of the intertidal green sea anemone, Anthopleura xanthogrammica, on the Oregon coast. Estuarine, Coastal and Shelf Science 13, 235–245.
Population characteristics of the intertidal green sea anemone, Anthopleura xanthogrammica, on the Oregon coast.Crossref | GoogleScholarGoogle Scholar |

Birch, L. C. (1948). The intrinsic rate of natural increase of an insect population. Journal of Animal Ecology 17, 15–26.
The intrinsic rate of natural increase of an insect population.Crossref | GoogleScholarGoogle Scholar |

Birkeland, C., and Dayton, P. K. (2005). The importance in fishery management of leaving the big ones. Trends in Ecology & Evolution 20, 356–358.
The importance in fishery management of leaving the big ones.Crossref | GoogleScholarGoogle Scholar |

Bonin, M. C., Harrison, H. B., Williamson, D. H., Frisch, A. J., Saenz-Agudelo, P., Berumen, M. L., and Jones, G. P. (2016). The role of marine reserves in the replenishment of a locally impacted population of anemonefish on the Great Barrier Reef. Molecular Ecology 25, 487–499.
The role of marine reserves in the replenishment of a locally impacted population of anemonefish on the Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar |

Bshary, R. (2003). The cleaner wrasse, Labroides dimidiatus, is a key organism for reef fish diversity at Ras Mohammed National Park, Egypt. Journal of Animal Ecology 72, 169–176.
The cleaner wrasse, Labroides dimidiatus, is a key organism for reef fish diversity at Ras Mohammed National Park, Egypt.Crossref | GoogleScholarGoogle Scholar |

Bucklin, A. (1987). Growth and asexual reproduction of the sea anemone Metridium: comparative laboratory studies of three species. Journal of Experimental Marine Biology and Ecology 110, 41–52.
Growth and asexual reproduction of the sea anemone Metridium: comparative laboratory studies of three species.Crossref | GoogleScholarGoogle Scholar |

Buston, P. M., and Garcia, M. B. (2007). An extraordinary life span estimate for the clown anemonefish Amphiprion percula. Journal of Fish Biology 70, 1710–1719.
An extraordinary life span estimate for the clown anemonefish Amphiprion percula.Crossref | GoogleScholarGoogle Scholar |

Cantrell, C. E., Henry, R. P., and Chadwick, N. E. (2015). Nitrogen transfer in a Caribbean mutualistic network. Marine Biology 162, 2327–2338.
Nitrogen transfer in a Caribbean mutualistic network.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvVyqs7bL&md5=cb4905b89e1f43b5fb5cd71c59fc1d02CAS |

Chadwick, N. E., and Arvedlund, M. (2005). Abundance of giant sea anemones and patterns of association with anemonefish in the northern Red Sea. Journal of the Marine Biological Association of the United Kingdom 85, 1287–1292.
Abundance of giant sea anemones and patterns of association with anemonefish in the northern Red Sea.Crossref | GoogleScholarGoogle Scholar |

Chadwick, N. E., Ďuriš, Z., and Horká, I. (2008). Biodiversity and behavior of shrimps and fishes symbiotic with sea anemones in the Gulf of Aqaba, northern Red Sea. In ‘The Improbable Gulf: History, Biodiversity, and Protection of the Gulf of Aqaba (Eilat)’. (Ed. F. D. Por.) pp. 209–223. (Magnes Press, Hebrew University: Jerusalem, Israel.)

Chadwick-Furman, N. E., and Spiegel, M. (2000). Abundance and asexual reproduction of the tropical corallimorpharian Rhodactis rhodostoma. Invertebrate Biology 119, 351–360.
Abundance and asexual reproduction of the tropical corallimorpharian Rhodactis rhodostoma.Crossref | GoogleScholarGoogle Scholar |

Chadwick-Furman, N. E., Goffredo, S., and Loya, Y. (2000a). Growth and population dynamic model of the reef coral Fungia granulosa Klunzinger, 1879 at Eilat, northern Red Sea. Journal of Experimental Marine Biology and Ecology 249, 199–218.
Growth and population dynamic model of the reef coral Fungia granulosa Klunzinger, 1879 at Eilat, northern Red Sea.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2sbitlSquw%3D%3D&md5=e580a8530eac833b5a693ad26dacabdeCAS |

Chadwick-Furman, N. E., Nir, I., and Spiegel, M. (2000b). Sexual reproduction in the tropical corallimorpharian Rhodactis rhodostoma. Invertebrate Biology 119, 361–369.
Sexual reproduction in the tropical corallimorpharian Rhodactis rhodostoma.Crossref | GoogleScholarGoogle Scholar |

Chomsky, O., Kamenir, Y., Hyams, M., Dubinsky, Z., and Chadwick-Furman, N. E. (2004). Effects of feeding regime on growth rate in the Mediterranean sea anemone Actinia equina (Linnaeus). Journal of Experimental Marine Biology and Ecology 299, 217–229.
Effects of feeding regime on growth rate in the Mediterranean sea anemone Actinia equina (Linnaeus).Crossref | GoogleScholarGoogle Scholar |

Cleveland, A., Verde, E. A., and Lee, R. W. (2011). Nutritional exchange in a tropical tripartite symbiosis: direct evidence for the transfer of nutrients from anemonefish to host anemone and zooxanthellae. Marine Biology 158, 589–602.
Nutritional exchange in a tropical tripartite symbiosis: direct evidence for the transfer of nutrients from anemonefish to host anemone and zooxanthellae.Crossref | GoogleScholarGoogle Scholar |

Courchamp, F., Clutton-Brock, T., and Grenfell, B. (1999). Inverse density dependence and the Allee effect. Trends in Ecology & Evolution 14, 405–410.
Inverse density dependence and the Allee effect.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2sbgvVynsA%3D%3D&md5=69203bcc91da71e6cbbe732508fce88eCAS |

Diamond, J. M. (1969). Avifaunal equilibria and species turnover rates on the channel islands of California. Proceedings of the National Academy of Sciences of the United States of America 64, 57–63.
Avifaunal equilibria and species turnover rates on the channel islands of California.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cngslSjtQ%3D%3D&md5=8160113af85eece1491ddd6c0a30f9bfCAS |

Dixon, A. K., Needham, D., Al-Horani, F. A., and Chadwick, N. E. (2014). Microhabitat use and photoacclimation in the clownfish sea anemone Entacmaea quadricolor. Journal of the Marine Biological Association of the United Kingdom 94, 473–480.
Microhabitat use and photoacclimation in the clownfish sea anemone Entacmaea quadricolor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXls1Whsr4%3D&md5=51e38a07815f748eca4a8f2d6f4b370eCAS |

Dunn, D. F. (1977). Dynamics of external brooding in the sea anemone Epictis Epiactis prolifera. Marine Biology 39, 41–49.
Dynamics of external brooding in the sea anemone Epictis Epiactis prolifera.Crossref | GoogleScholarGoogle Scholar |

Edmunds, P. J. (2010). Population biology of Porites astreoides and Diploria strigosa on a shallow Caribbean reef. Marine Ecology Progress Series 418, 87–104.
Population biology of Porites astreoides and Diploria strigosa on a shallow Caribbean reef.Crossref | GoogleScholarGoogle Scholar |

Environmental Law Institute (1993). ‘Protecting the Gulf of Aqaba: a Regional Environmental Challenge.’ (ELI: Washington, DC, USA.)

Fautin, D. G., and Allen, G. R. (1997). ‘Anemonefishes and Their Host Sea Anemones: A Guide for Aquarists and Divers’, revised edn. (Western Australian Museum: Perth, WA, Australia.)

Fricke, H. W. (1983). Social control of sex: field experiments with the anemonefish Amphiprion bicinctus. Zeitschrift für Tierpsychologie 61, 71–77.
Social control of sex: field experiments with the anemonefish Amphiprion bicinctus.Crossref | GoogleScholarGoogle Scholar |

Frisch, A. J., Rizzari, J. R., Munkres, K. P., and Hobbs, J. A. (2016). Anemonefish depletion reduces survival, growth, reproduction and fishery productivity of mutualistic anemone-anemonefish colonies. Coral Reefs 35, 375–386.
Anemonefish depletion reduces survival, growth, reproduction and fishery productivity of mutualistic anemone-anemonefish colonies.Crossref | GoogleScholarGoogle Scholar |

Gascoigne, J., and Lipcius, R. N. (2004). Allee effects in marine systems. Marine Ecology Progress Series 269, 49–59.
Allee effects in marine systems.Crossref | GoogleScholarGoogle Scholar |

Godinot, C., and Chadwick, N. E. (2009). Phosphate excretion by anemonefish and uptake by giant sea anemones: demand outstrips supply. Bulletin of Marine Science 85, 1–9.

Godwin, J., and Fautin, D. G. (1992). Defense of host actinians by anemonefishes. Copeia 3, 903–908.

Grutter, A. S., Murphy, J. M., and Choat, J. H. (2003). Cleaner fish drives local fish diversity on coral reefs. Current Biology 13, 64–67.
Cleaner fish drives local fish diversity on coral reefs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltlarsQ%3D%3D&md5=fb1ea357627a16865afe84de5fcf33d3CAS |

Guo, C., Hwang, J., and Fautin, D. G. (1996). Host selection by shrimps symbiotic with sea anemones: a field survey and experimental laboratory analysis. Journal of Experimental Marine Biology and Ecology 202, 165–176.
Host selection by shrimps symbiotic with sea anemones: a field survey and experimental laboratory analysis.Crossref | GoogleScholarGoogle Scholar |

Guzner, B., Novoplansky, A., and Chadwick, N. E. (2007). Population dynamics of the reef-building coral Acropora hemprichii as an indicator of reef condition. Marine Ecology Progress Series 333, 143–150.
Population dynamics of the reef-building coral Acropora hemprichii as an indicator of reef condition.Crossref | GoogleScholarGoogle Scholar |

Guzner, B., Novplansky, A., Shalit, O., and Chadwick, N. E. (2010). Indirect impacts of recreational scuba diving: patterns of growth and predation in branching stony corals. Bulletin of Marine Science 86, 727–742.

Hattori, A. (2002). Small and large anemonefishes can coexist using the same patchy resources on a coral reef, before habitat destruction. Journal of Animal Ecology 71, 824–831.
Small and large anemonefishes can coexist using the same patchy resources on a coral reef, before habitat destruction.Crossref | GoogleScholarGoogle Scholar |

Hattori, A. (2006). Vertical and horizontal distribution patterns of the giant sea anemone Heteractis crispa with symbiotic anemonefish on a fringing coral reef. Journal of Ethology 24, 51–57.
Vertical and horizontal distribution patterns of the giant sea anemone Heteractis crispa with symbiotic anemonefish on a fringing coral reef.Crossref | GoogleScholarGoogle Scholar |

Hawkins, J. P., and Roberts, C. M. (1993). Effects of recreational scuba diving on coral reefs: trampling on reef-flat communities. Journal of Applied Ecology 30, 25–30.
Effects of recreational scuba diving on coral reefs: trampling on reef-flat communities.Crossref | GoogleScholarGoogle Scholar |

Hill, R., Fernance, C., Wilkinson, S. P., Davy, S. K., and Scott, A. (2014). Symbiont shuffling during thermal bleaching and recovery in the sea anemone Entacmaea quadricolor. Marine Biology 161, 2931–2937.
Symbiont shuffling during thermal bleaching and recovery in the sea anemone Entacmaea quadricolor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFWkt7vJ&md5=60f442d1f3b1e370959fd10890b167acCAS |

Hirose, Y. (1985). Habitat, distribution and abundance of coral reef sea anemones (Actiniidae and Stichodactylidae) in Sesoko Island, Okinawa, with notes of expansion and contraction behavior. Galaxea 4, 113–127.

Hobbs, J. P. A., Frisch, A. J., Ford, B. M., Thums, M., Saenz-Agudelo, P., Furby, K. A., and Berumen, M. I. (2013). Taxonomic, spatial and temporal patterns of bleaching in anemones inhabited by anemonefishes. PLoS One 8, e70966.
Taxonomic, spatial and temporal patterns of bleaching in anemones inhabited by anemonefishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlamsrjP&md5=1958b70a320a4a21353b66e4db38b567CAS |

Holbrook, S. J., and Schmitt, R. J. (2005). Growth, reproduction and survival of a tropical sea anemone (Actiniaria): benefits of hosting anemonefish. Coral Reefs 24, 67–73.
Growth, reproduction and survival of a tropical sea anemone (Actiniaria): benefits of hosting anemonefish.Crossref | GoogleScholarGoogle Scholar |

Huebner, L. K., and Chadwick, N. E. (2012). Reef fishes use sea anemones as visual cues for cleaning interactions with shrimp. Journal of Experimental Marine Biology and Ecology 416–417, 237–242.
Reef fishes use sea anemones as visual cues for cleaning interactions with shrimp.Crossref | GoogleScholarGoogle Scholar |

Huebner, L. K., Dailey, B., Titus, B. M., Khalaf, M., and Chadwick, N. E. (2012). Host preference and habitat segregation among Red Sea anemonefish: effects of sea anemone traits and fish life stages. Marine Ecology Progress Series 464, 1–15.
Host preference and habitat segregation among Red Sea anemonefish: effects of sea anemone traits and fish life stages.Crossref | GoogleScholarGoogle Scholar |

Hughes, T. P. (1984). Population dynamics based on individual size rather than age: a general model with a reef coral example. American Naturalist 123, 778–795.
Population dynamics based on individual size rather than age: a general model with a reef coral example.Crossref | GoogleScholarGoogle Scholar |

Hughes, T. P., and Jackson, J. B. C. (1985). Population dynamics and life histories of foliaceous corals. Ecological Monographs 55, 141–166.
Population dynamics and life histories of foliaceous corals.Crossref | GoogleScholarGoogle Scholar |

Hunter, T. (1984). The energetics of asexual reproduction: pedal laceration in the symbiotic sea anemone Aiptasia pulchella (Cargren, 1943). Journal of Experimental Marine Biology and Ecology 83, 127–147.
The energetics of asexual reproduction: pedal laceration in the symbiotic sea anemone Aiptasia pulchella (Cargren, 1943).Crossref | GoogleScholarGoogle Scholar |

Jennison, B. L. (1981). Reproduction in three species of sea anemones from Key West, Florida. Canadian Journal of Zoology 59, 1708–1719.
Reproduction in three species of sea anemones from Key West, Florida.Crossref | GoogleScholarGoogle Scholar |

Jones, A. M., Gardner, S., and Sinclair, W. (2008). Losing ‘Nemo’: bleaching and collection appear to reduce inshore populations of anemonefishes. Journal of Fish Biology 73, 753–761.
Losing ‘Nemo’: bleaching and collection appear to reduce inshore populations of anemonefishes.Crossref | GoogleScholarGoogle Scholar |

Khalaf, M. A., and Kochzius, M. (2002). Community structure and biogeography of shore fishes in the Gulf of Aqaba, Red Sea. Helgoland Marine Research 55, 252–284.
Community structure and biogeography of shore fishes in the Gulf of Aqaba, Red Sea.Crossref | GoogleScholarGoogle Scholar |

Kotb, M. M. A., Abdulaziz, M., Al-Agwan, Z., Alshaikh, K., Al-Yami, H., Banajah, A., Devamed, L., Eisinger, M., Eltayeb, M., Hassan, M., Heiss, G., Howe, S., Kemp, J., Klaus, R., Krupp, F., Mohamed, N., Rouphael, T., Turner, J., and Zajonz, U. (2004). Status of coral reefs in the Red Sea and Gulf of Aden in 2004. In ‘Status of Coral Reefs of the World: 2004’. (Ed. C. Wilkinson.) pp. 137–154. (Australian Institute of Marine Science: Townsville, Qld, Australia.)

Leslie, P. H. (1945). On the use of matrices in certain population mathematics. Biometrika 33, 183–212.
On the use of matrices in certain population mathematics.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaH28%2FisV2nsg%3D%3D&md5=f3791e33f9823a0aad7963d57fed4907CAS |

Loya, Y. (2004). The coral reefs of Eilat – past, present and future: three decades of coral community structure studies. In ‘Coral Health and Disease’. (Eds E. Rosenberg and Y. Loya.) pp. 1–34. (Springer: New York, NY, USA.)

Madduppa, H. H., von Juterzenka, K., Syakir, M., and Kochzius, M. (2014). Socio-economy of marine ornamental fishery and its impact on the population structure of the clown anemonefish Amphiprion ocellaris and its host anemones in Spermonde Archipelago, Indonesia. Ocean and Coastal Management 100, 41–50.
Socio-economy of marine ornamental fishery and its impact on the population structure of the clown anemonefish Amphiprion ocellaris and its host anemones in Spermonde Archipelago, Indonesia.Crossref | GoogleScholarGoogle Scholar |

McVay, M. J. (2015). Population dynamics of clownfish sea anemones: patterns of decline, symbiosis with anemonefish, and management for sustainability. M.Sc. Thesis, Auburn University, Auburn, AL, USA. Available at https://etd.auburn.edu/handle/10415/4940 [Verified 7 March 2017].

Mitchell, J. S., and Dill, L. M. (2005). Why is group size correlated with the size of the host sea anemone in the false clown anemonefish? Canadian Journal of Zoology 83, 372–376.
Why is group size correlated with the size of the host sea anemone in the false clown anemonefish?Crossref | GoogleScholarGoogle Scholar |

Moyer, J. T. (1980). Influence of temperate waters on the behavior of the tropical anemonefish Amphiprion clarkii at Miyake-jima, Japan. Bulletin of Marine Science 30, 261–272.

Mumby, P. J., and Harborne, A. R. (2010). Marine reserves enhance the recovery of corals on Caribbean reefs. PLoS One 5, e8657.
Marine reserves enhance the recovery of corals on Caribbean reefs.Crossref | GoogleScholarGoogle Scholar |

Mumby, P. J., Harborne, A. R., Williams, J., Kappel, C. V., Brumbaugh, D. R., Micheli, F., Holmes, K. E., Dahlgren, C. P., Paris, C. B., and Blackwell, P. G. (2007). Trophic cascade facilitates coral recruitment in a marine reserve. Proceedings of the National Academy of Sciences of the United States of America 104, 8362–8367.
Trophic cascade facilitates coral recruitment in a marine reserve.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtVertbg%3D&md5=bf69f52dd62d22c9e8f5746c0b73aeeaCAS |

Munday, P. L. (2004). Habitat loss, resource specialization, and extinction on coral reefs. Global Change Biology 10, 1642–1647.
Habitat loss, resource specialization, and extinction on coral reefs.Crossref | GoogleScholarGoogle Scholar |

O’Reilly, E. (2015). Demography of the corkscrew sea anemone Bartholomea annulata in the Florida Keys and in laboratory culture: a giant sea anemone under pressure. M.Sc. Thesis, Auburn University, Auburn, AL, USA. Available at https://etd.auburn.edu/handle/10415/4972 [Verified 7 March 2017].

O’Reilly, E. E., and Chadwick, N. E. (2017). Population dynamics of corkscrew sea anemones Bartholomea annulata in the Florida Keys. Marine Ecology Progress Series 567, 109–123.
Population dynamics of corkscrew sea anemones Bartholomea annulata in the Florida Keys.Crossref | GoogleScholarGoogle Scholar |

Ottaway, J. R. (1978). Population ecology of the intertidal anemone Actinia tenebrosa. I. Pedal locomotion and intraspecific aggression. Marine and Freshwater Research 29, 787–802.
Population ecology of the intertidal anemone Actinia tenebrosa. I. Pedal locomotion and intraspecific aggression.Crossref | GoogleScholarGoogle Scholar |

Ottaway, J. R. (1979). Population ecology of the intertidal anemone Actinia tenebrosa. III. Dynamics and environmental factors. Marine and Freshwater Research 30, 41–62.
Population ecology of the intertidal anemone Actinia tenebrosa. III. Dynamics and environmental factors.Crossref | GoogleScholarGoogle Scholar |

Ottaway, J. R. (1980). Population ecology of the intertidal anemone Actinia tenebrosa. IV. Growth rates and longevities. Marine and Freshwater Research 31, 385–395.
Population ecology of the intertidal anemone Actinia tenebrosa. IV. Growth rates and longevities.Crossref | GoogleScholarGoogle Scholar |

Planes, S., Jones, G. P., and Thorrold, S. R. (2009). Larval dispersal connects fish populations in a network of marine protected areas. Proceedings of the National Academy of Sciences of the United States of America 106, 5693–5697.
Larval dispersal connects fish populations in a network of marine protected areas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkvFOns70%3D&md5=f67540689973b45668bc6763dd6bbb4bCAS |

Porat, D., and Chadwick-Furman, N. E. (2004). Effects of anemonefish on giant sea anemones: expansion behavior, growth, and survival. Hydrobiologia 530–531, 513–520.
Effects of anemonefish on giant sea anemones: expansion behavior, growth, and survival.Crossref | GoogleScholarGoogle Scholar |

Portman, M. E. (2007). Zoning design for cross-border marine protected areas: the Red Sea Marine Peace Park case study. Ocean and Coastal Management 50, 499–522.
Zoning design for cross-border marine protected areas: the Red Sea Marine Peace Park case study.Crossref | GoogleScholarGoogle Scholar |

Roberts, C. M., and Hawkins, J. P. (1999). Extinction risk in the sea. Trends in Ecology & Evolution 14, 241–246.
Extinction risk in the sea.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2sbgsFeisg%3D%3D&md5=3e17b1385ffa93c3fb5295f5b07b371fCAS |

Rogers, C. S. (1983). Sublethal and lethal effects of sediments applied to common Caribbean reef corals in the field. Marine Pollution Bulletin 14, 378–382.
Sublethal and lethal effects of sediments applied to common Caribbean reef corals in the field.Crossref | GoogleScholarGoogle Scholar |

Roopin, M., and Chadwick, N. E. (2009). Benefits to host sea anemones from ammonia contributions of resident anemonefish. Journal of Experimental Marine Biology and Ecology 370, 27–34.
Benefits to host sea anemones from ammonia contributions of resident anemonefish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvFGrtbs%3D&md5=ddd80836c2aa7a416585bbbeb6459510CAS |

Saenz-Agudelo, P., Jones, G. P., Thorrold, S. R., and Planes, S. (2011). Detrimental effects of host anemone bleaching on anemonefish populations. Coral Reefs 30, 497–506.
Detrimental effects of host anemone bleaching on anemonefish populations.Crossref | GoogleScholarGoogle Scholar |

Scott, A., and Harrison, P. (2007a). Broadcast spawning of two species of sea anemone, Entacmaea quadricolor and Heteractis crispa, that host anemonefish. Invertebrate Reproduction & Development 50, 163–171.
Broadcast spawning of two species of sea anemone, Entacmaea quadricolor and Heteractis crispa, that host anemonefish.Crossref | GoogleScholarGoogle Scholar |

Scott, A., and Harrison, P. L. (2007b). Embryonic and larval development of the host sea anemones Entacmaea quadricolor and Heteractis crispa. The Biological Bulletin 213, 110–121.
Embryonic and larval development of the host sea anemones Entacmaea quadricolor and Heteractis crispa.Crossref | GoogleScholarGoogle Scholar |

Scott, A., and Harrison, P. L. (2009). Gametogenic and reproductive cycles of the sea anemone, Entacmaea quadricolor. Marine Biology 156, 1659–1671.
Gametogenic and reproductive cycles of the sea anemone, Entacmaea quadricolor.Crossref | GoogleScholarGoogle Scholar |

Scott, A., Malcolm, H. A., Damiano, C., and Richardson, D. L. (2013). Long-term increases in abundance of anemonefish and their host sea anemones in an Australian marine protected area. Marine and Freshwater Research 62, 187–196.
Long-term increases in abundance of anemonefish and their host sea anemones in an Australian marine protected area.Crossref | GoogleScholarGoogle Scholar |

Sebens, K. P. (1981). Reproductive ecology of the intertidal sea anemones Anthopleura xanthogrammica (Brandt) and A. elegantissima (Brandt): body size, habitat, and sexual reproduction. Journal of Experimental Marine Biology and Ecology 54, 225–250.
Reproductive ecology of the intertidal sea anemones Anthopleura xanthogrammica (Brandt) and A. elegantissima (Brandt): body size, habitat, and sexual reproduction.Crossref | GoogleScholarGoogle Scholar |

Shlesinger, T., and Loya, Y. (2016). Recruitment, mortality, and resilience potential of scleractinian corals at Eilat, Red Sea. Coral Reefs 35, 1357–1368.
Recruitment, mortality, and resilience potential of scleractinian corals at Eilat, Red Sea.Crossref | GoogleScholarGoogle Scholar |

Shuman, C. S., Hodgson, G., and Ambrose, R. F. (2005). Population impacts of collecting sea anemones and anemonefish for the marine aquarium trade in the Philippines. Coral Reefs 24, 564–573.
Population impacts of collecting sea anemones and anemonefish for the marine aquarium trade in the Philippines.Crossref | GoogleScholarGoogle Scholar |

Szczebak, J. T., Henry, R. P., Al-Horani, F. A., and Chadwick, N. E. (2013). Anemonefish oxygenate their anemone hosts at night. The Journal of Experimental Biology 216, 970–976.
Anemonefish oxygenate their anemone hosts at night.Crossref | GoogleScholarGoogle Scholar |

Szmant, A. M. (2002). Nutrient enrichment on coral reefs: is it a major cause of coral reef decline? Estuaries 25, 743–766.
Nutrient enrichment on coral reefs: is it a major cause of coral reef decline?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XosVagsb8%3D&md5=280f14b49f977bd063201b137e74e905CAS |

Verde, E. A., Cleveland, A., and Lee, R. W. (2015). Nutritional exchange in a tropical tripartite symbiosis II: direct evidence for the transfer of nutrients from host anemone and zooxanthellae to anemonefish. Marine Biology 162, 2409–2429.

Vermeij, M. J. A. (2006). Early life-history dynamics of Caribbean coral species on artificial substratum: the importance of competition, growth and variation in life-history strategy. Coral Reefs 25, 59–71.
Early life-history dynamics of Caribbean coral species on artificial substratum: the importance of competition, growth and variation in life-history strategy.Crossref | GoogleScholarGoogle Scholar |

Wabnitz, C., Taylor, M., Green, E., and Razak, T. (2003). From ocean to aquarium: the global trade in marine ornamental species. (United Nations Environment Programme, World Conservation Monitoring Centre: Cambridge, UK.) Available at http://ia800502.us.archive.org/25/items/fromoceantoaquar03wabn/fromoceantoaquar03wabn.pdf [Verified 5 May 2017].

Warner, R. R., and Chesson, P. L. (1985). Coexistence mediated by recruitment fluctuations: a field guide to the storage effect. American Naturalist 125, 769–787.
Coexistence mediated by recruitment fluctuations: a field guide to the storage effect.Crossref | GoogleScholarGoogle Scholar |

Wielgus, J., Chadwick-Furman, N. E., and Dubinsky, Z. (2004). Coral cover and partial mortality on anthropogenically impacted coral reefs at Eilat, northern Red Sea. Marine Pollution Bulletin 48, 248–253.
Coral cover and partial mortality on anthropogenically impacted coral reefs at Eilat, northern Red Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXht12rtb0%3D&md5=7c52cc8efae9166e55756f31a8547e0aCAS |