Abstract
Characterizing spatial patterns of occurrence can lend insight into the ecological processes that determine how individuals are distributed within their environment. When microhabitat specialist fishes and their invertebrate hosts are co-distributed, disentangling their respective spatial patterns is a complex problem. Here, we use point pattern analysis (PPA) to examine the spatial distributions of a host sponge Aplysina fistularis and its resident goby Elacatinus lori from a fully censused plot at Curlew Cay, Belize (16°47′23″N 88°04′33″W), sampled in summer 2011. The PPA approach allowed us to disentangle the spatial distribution of sponges and the spatial distribution of goby-occupied sponges. After controlling for depth and the distribution of hard substrate, we found that the sponges were clustered at small scales (< 4.5 m) within the censused area. After controlling for sponge clustering, we found that goby-occupied sponges were neither clustered nor over-dispersed within the censused area. Two fish age classes, recent settlers and established residents, were closely associated at small scales (< 3.5 m). We discuss alternative ecological and behavioral hypotheses for the cause of these spatial patterns. Despite the limited application of PPA in marine ecology, we demonstrate the potential use of this statistical analysis in disentangling the spatial structure of co-distributed populations and providing preliminary insights into the processes that may account for their respective distributions.
References
Alzate A, Zapata FA, Giraldo A (2014) A comparison of visual and collection-based methods for assessing community structure of coral reef fishes in the Tropical Eastern Pacific. Rev Biol Trop 62:359. https://doi.org/10.15517/rbt.v62i0.16361
Baddeley A, Turner R (2005) Spatstat an R package for analyzing spatial point patterns. J Stat Softw 12:1–42. https://doi.org/10.18637/jss.v012.i06
Beldade R, Gonçalves EJ (2007) An interference visual census technique applied to cryptobenthic fish assemblages. Vie Milieu 57:61–65
Buston PM (2003) Forcible eviction and prevention of recruitment in the clown anemonefish. Behav Ecol 14:576–582. https://doi.org/10.1093/beheco/arg036
Chausson J, Srinivasan M, Jones GP (2018) Host anemone size as a determinant of social group size and structure in the orange clownfish (Amphiprion percula). PeerJ 6:e5841. https://doi.org/10.7717/peerj.5841
Coker DJ, DiBattista JD, Sinclair-Taylor TH, Berumen ML (2018) Spatial patterns of cryptobenthic coral-reef fishes in the Red Sea. Coral Reefs 37:193–199. https://doi.org/10.1007/s00338-017-1647-9
Colby DR, Fonseca MS (1984) Population dynamics, spatial dispersion, and somatic growth of the sand fiddler crab Uca pugilator. Mar Ecol Prog Ser 16:269–279. https://doi.org/10.3354/meps016269
Cole RG, Syms C (1999) Using spatial pattern analysis to distinguish causes of mortality: an example from kelp in north-eastern New Zealand. J Ecol 87:963–972. https://doi.org/10.1046/j.1365-2745.1999.00418.x
Colin PL (2002) A new species of sponge-dwelling Elacatinus (Pisces: Gobiidae) from the western Caribbean. Zootaxa 106:1–7. https://doi.org/10.11646/zootaxa.106.1.1
D’Aloia CC, Majoris JE, Buston PM (2011) Predictors of the distribution and abundance of a tube sponge and its resident goby. Coral Reefs 30:777–786. https://doi.org/10.1007/s00338-011-0755-1
D’Aloia CC, Bogdanowicz SM, Francis RK, Majoris JE, Harrison RG, Buston PM (2015) Patterns, causes, and consequences of marine larval dispersal. Proc Natl Acad Sci USA 112:13940–13945. https://doi.org/10.1073/pnas.1513754112
D’Aloia CC, Xuereb A, Fortin MJ, Bogdanowicz SM, Buston PM (2018) Limited dispersal explains the spatial distribution of siblings in a reef fish population. Mar Ecol Prog Ser 607:143–154. https://doi.org/10.3354/meps12792
Dale MR, Fortin MJ (2014) Spatial analysis: a guide for ecologists. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511978913
Depczynski M, Bellwood DR (2003) The role of cryptobenthic reef fishes in coral reef trophodynamics. Mar Ecol Prog Ser 256:183–191. https://doi.org/10.3354/meps256183
Diaz MC, Rützler K (2001) Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci 69:535–546
Elliott JK, Mariscal RN (2001) Coexistence of nine anemonefish species: differential host and habitat utilization, size and recruitment. Mar Biol 138:123–136. https://doi.org/10.1007/s002270000441
Endean R, Cameron AM, Fox HE, Tilbury R, Gunthrope L (1997) Massive corals are regularly spaced: pattern in a complex assemblage of corals. Mar Ecol Prog Ser 152:119–130. https://doi.org/10.3354/meps152119
Feary DA (2007) The influence of resource specialization on the response of reef fish to coral disturbance. Mar Biol 153:153–161. https://doi.org/10.1007/s00227-007-0791-0
Harborne AR, Jelks HL, Smith-Vaniz WF, Rocha LA (2012) Abiotic and biotic controls of cryptobenthic fish assemblages across a Caribbean seascape. Coral Reefs 31:977–990. https://doi.org/10.1007/s00338-012-0938-4
Hayes FE, Trimm NA (2008) Distributional ecology of the anemone shrimp Periclimenes rathbunae associating with the sea anemone Stichodactyla helianthus at Tobago, West Indies. Nauplius 16:73–77
Illian J, Penttinen A, Stoyan H, Stoyan D (2008) Statistical analysis and modelling of spatial point patterns, vol 70. Wiley, New York. https://doi.org/10.1002/9780470725160
Kane CN, Brooks AJ, Holbrook SJ, Schmitt RJ (2009) The role of microhabitat preference and social organization in determining the spatial distribution of a coral reef fish. Environ Biol Fishes 84:1–10. https://doi.org/10.1007/s10641-008-9377-z
Karlson RH, Cornell HV, Hughes TP (2007) Aggregation influences coral species richness at multiple spatial scales. Ecology 88:170–177. https://doi.org/10.1890/0012-9658(2007)88%5b170:AICSRA%5d2.0.CO;2
Liversage K, Benkendorff K (2013) A preliminary investigation of diversity, abundance, and distributional patterns of chitons in intertidal boulder fields of differing rock type in South Australia. Molluscan Res 33:24–33. https://doi.org/10.1080/13235818.2012.754145
Majoris JE, D’Aloia CC, Francis RK, Buston PM (2018) Differential persistence favors habitat preferences that determine the distribution of a reef fish. Behav Ecol 29:429–439. https://doi.org/10.1093/beheco/arx189
Maldonado M, Riesgo A (2008) Reproduction in the phylum Porifera: a synoptic overview. Treballs de la SCB 59:29–49
Maldonado M, Young C (1996) Effects of physical factors on larval behavior, settlement and recruitment of four tropical demosponges. Mar Ecol Prog Ser 138:169–180. https://doi.org/10.3354/meps138169
Melles SJ, Badzinski D, Fortin M-J, Csillag F, Lindsay K (2009) Disentangling habitat and social drivers of nesting patterns in songbirds. Landsc Ecol 24:519–531. https://doi.org/10.1007/s10980-009-9329-9
Miller PJ (1979) Adaptiveness and implications of small size in teleosts. Symp Zool Soc 44:263–306
Mitchel A (2005) The ESRI guide to GIS analysis, volume 2: spatial measurements and statistics. Environmental Systems Research Institute, Inc, Redlands
Munday PL, Jones GP (1998) The ecological implications of small body size among coral-reef fishes. Oceanogr Mar Biol 36:373–411
Munday PL, Jones GP, Caley MJ (1997) Habitat specialisation and the distribution and abundance of coral-dwelling gobies. Mar Ecol Prog Ser 152:227–239. https://doi.org/10.3354/meps152227
Nizinski MS (1989) Ecological distribution, demography and behavioral observations on Periclimenes anthophilus, an atypical symbiotic cleaner shrimp. Bull Mar Sci 45:174–188
Pineda J, Porri F, Starczak V, Blythe J (2010) Causes of decoupling between larval supply and settlement and consequences for understanding recruitment and population connectivity. J Exp Mar Biol Ecol 392:9–21. https://doi.org/10.1016/j.jembe.2010.04.008
Porri F, McQuaid DM, Radloff S (2006) Spatio-temporal variability of larval abundance and settlement of Perna perna: differential delivery of mussels. Mar Ecol Prog Ser 315:141–150. https://doi.org/10.1016/j.jembe.2010.04.008
Ripley BD (1988) Statistical inference for spatial processes. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511624131
Russo AR (1979) Dispersion and food differences between two populations of the sea urchin Strongylocentrotus franciscanus. J Biogeogr 1:407–414. https://doi.org/10.2307/3038092
Sale PF (1972) Influence of corals in the dispersion of the pomacentrid fish, Dascyllus aruanus. Ecology 53:741–744. https://doi.org/10.2307/1934795
Sale PF, Douglas WA (1981) Precision and accuracy of visual census technique for fish assemblages on coral patch reefs. Environ Biol Fish 6:333–339. https://doi.org/10.1007/BF00005761
Stimson J (1974) An analysis of the pattern of dispersion of the hermatypic coral Pocillopora meandrina var. nobilis Verril. Ecology 55:445–449. https://doi.org/10.2307/1935234
Taylor PD, Wilson MA (2003) Palaeoecology and evolution of marine hard substrate communities. Earth Sci Rev 62:1–103. https://doi.org/10.1016/S0012-8252(02)00131-9
Tolimieri N (1998) The relationship among microhabitat characteristics, recruitment and adult abundance in the stoplight parrot-fish, Sparisoma viride, at three spatial scales. Bull Mar Sci 62:253–268
Wagner HH, Fortin M-J (2005) Spatial analysis of landscapes: concepts and statistics. Ecology 86:1975–1987. https://doi.org/10.1890/04-0914
Wiegand T, Moloney KA (2013) Handbook of spatial point-pattern analysis in ecology. Chapman and Hall/CRC Press, Boca Raton
Wilkinson CR, Evans E (1989) Sponge distribution across Davies Reef, Great Barrier Reef, relative to location, depth, and water movement. Coral Reefs 8:1–7. https://doi.org/10.1007/BF00304685
Willis TJ (2001) Visual census methods underestimate density and diversity of cryptic reef fishes. J Fish Biol 59:1408–1411. https://doi.org/10.1111/j.1095-8649.2001.tb00202.x
Wirtz P (1997) Crustacean symbionts of the sea anemone Telmatactis cricoides at Madeira and the Canary Islands. J Zool 242:799–811. https://doi.org/10.1111/j.1469-7998.1997.tb05827.x
Wulff JL (1985) Dispersal and survival of fragments of coral reef sponges. Proc Fifth Int Coral Reef Congr 5:119–124
Zea S (1993) Recruitment of demosponges (Porifera, Demospongiae) in rocky and coral reef habitats of Santa Marta, Colombian Caribbean. Mar Ecol 14:1–21. https://doi.org/10.1111/j.1439-0485.1993.tb00361.x
Acknowledgements
The authors thank the major funding source for this fieldwork (start-up grant for PMB provided by Boston University). We thank Udel Foreman, John Majoris, Alissa Rickborn and Marian Wong for assistance in the field; Robin Francis for sharing unpublished data; and John Finnerty and two anonymous reviewers for comments on this manuscript.
Funding
All applicable international, national, and institutional guidelines for fieldwork, sampling, care, and use of organisms for the study and all necessary approvals have been obtained via Boston University IACUC protocol #10-036 and the Belize Fisheries Department. Funding was provided by a start-up award from the Trustees of Boston University, and by NSF awards OCE-1260424 and OCE-1459546, to PMB.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
During the writing of this manuscript, KCL was supported by a Warren McLeod Fellowship and a Teaching Fellowship at Boston University, and CCD was supported by a Natural Sciences and Engineering Research Council of Canada strategic grant to M-JF. All authors declare that we have neither conflict of interest with funding sources nor the submission of this manuscript.
Additional information
Responsible Editor: D. Goulet.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewed by K. Liversage and an undisclosed expert.
Rights and permissions
About this article
Cite this article
Lesneski, K.C., D’Aloia, C.C., Fortin, MJ. et al. Disentangling the spatial distributions of a sponge-dwelling fish and its host sponge. Mar Biol 166, 66 (2019). https://doi.org/10.1007/s00227-019-3517-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-019-3517-1