Testing the waters to find the ‘goldilocks’ zone: fine-scale movement of Mustelus mustelus in relation to environmental cues
Charlene da Silva A E , Sven E. Kerwath A B , Henning Winker A , Stephen J. Lamberth A D , Colin G. Attwood B , Chris G. Wilke A and Tor F. Næsje CA Department of Forestry and Fisheries and the Environment, Vlaeberg, Cape Town, 8018, South Africa.
B Biological Sciences Department, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa.
C Norwegian Institute for Nature Research, PO Box 5685 Torgarden, NO-7485 Trondheim, Norway.
D Institute for Coastal and Marine Research, Nelson Mandela University, Port Elizabeth, 6301, South Africa.
E Corresponding author. Email: cdasilva@environentgov.za; mustelusmustelus@gmail.com
Marine and Freshwater Research 73(1) 110-124 https://doi.org/10.1071/MF20369
Submitted: 17 December 2020 Accepted: 10 September 2021 Published: 29 October 2021
Abstract
The fine-scale movement of Mustelus mustelus in relation to environmental conditions was investigated at various temporal scales with acoustic telemetry and temperature–depth transmitters inside a coastal marine protected area in South Africa. Twenty-four sharks were equipped with acoustic tags and logged by an array of 28 acoustic receivers from November 2006 to November 2008. Generalised additive and generalised additive mixed models (GAMMs) were used to explain patterns of movement in terms of the environmental conditions related to temperature, the rate of change of temperature, tidal flow, diel cycle and moon phase. The most important environmental parameters affecting movement and direction of movement were related to absolute temperature and changes in temperature at the position of the shark. The movement of M. mustelus was not affected by tide and only minimally affected by the diel cycle, suggesting behavioural thermoregulation as the ultimate cause of the movements. M. mustelus preferred temperatures from 18 to 22°C, as determined by GAMMs for environmental conditions experienced in summer. The combination of the thermal environment, rich feeding grounds and protective effect of the Langebaan Marine Protected Area may explain the high abundance and regular occurrence of M. mustelus within this marine protected area.
Keywords: chondrichthyes, environmental cues, marine protected area, movements, smoothhound sharks.
References
Ackerman, J. T., Kondratieff, M. C., Matern, S. A., and Cech, J. J. (2000). Tidal influence on spatial dynamics of leopard sharks, Triakis semifasciata, in Tomales Bay, California. Environmental Biology of Fishes 58, 33–43.| Tidal influence on spatial dynamics of leopard sharks, Triakis semifasciata, in Tomales Bay, California.Crossref | GoogleScholarGoogle Scholar |
Andrews, K. S., Williams, G. D., Farrer, D., Tolimieri, N., Harvey, C. J., Bargmann, G., and Levin, P. S. (2009). Diel activity pattern of sixgill sharks, Hexanchus griseus; the ups and downs of an apex predator. Animal Behaviour 78, 525–536.
| Diel activity pattern of sixgill sharks, Hexanchus griseus; the ups and downs of an apex predator.Crossref | GoogleScholarGoogle Scholar |
Attwood, C. G., Cowley, P. D., Kerwath, S. E., Næsje, T. F., Økland, F., and Thorstad, E. B. (2007). First tracking of white stumpnose Rhabdosargus globiceps (Sparidae) in a South African marine protected area. African Journal of Marine Science 29, 147–151.
| First tracking of white stumpnose Rhabdosargus globiceps (Sparidae) in a South African marine protected area.Crossref | GoogleScholarGoogle Scholar |
Barnett, A., and Semmens, J. M. (2012). Sequential movement into coastal habitats and high spatial overlap of predator and prey suggest high predation pressure in protected areas. Oikos 121, 882–890.
| Sequential movement into coastal habitats and high spatial overlap of predator and prey suggest high predation pressure in protected areas.Crossref | GoogleScholarGoogle Scholar |
Barnett, A., Abrantes, K., Stevens, J. D., Yick, J. L., Frusher, S. D., and Semmens, J. M. (2010). Predator–prey relationships and foraging ecology of a marine apex predator with a wide temperate distribution. Marine Ecology Progress Series 416, 189–200.
| Predator–prey relationships and foraging ecology of a marine apex predator with a wide temperate distribution.Crossref | GoogleScholarGoogle Scholar |
Bernal, D., and Lowe, C. G. (2015). Field physiology: field physiology of elasmobranch fishes. In ‘Fish Physiology: Physiology of Elasmobranch Fishes: Structure and Interaction with Environment’. (Eds R. E. Shadwick, A. P. Farrel, and C. J. Brauner.) pp. 311–346. (Elsevier Press: Oxford, UK.)
Campos, B. R., Fish, M. A., Jones, G., Riley, R. W., Allen, P. J., Klimley, P. A., Cech, J. J., and Kelly, J. T. (2009). Movements of brown smoothhounds, Mustelus henlei, in Tomales Bay, California. Environmental Biology of Fishes 85, 3–13.
| Movements of brown smoothhounds, Mustelus henlei, in Tomales Bay, California.Crossref | GoogleScholarGoogle Scholar |
Carey, F. G., Scharold, J. V., and Kalmijn, A. J. (1990). Movements of blue sharks (Prionace glauca) in depth and course. Marine Biology 106, 329–342.
| Movements of blue sharks (Prionace glauca) in depth and course.Crossref | GoogleScholarGoogle Scholar |
Casterlin, M. E., and Reynolds, W. W. (1979). Shark thermoregulation. Comparative Biochemistry and Physiology – A. Physiology 64, 451–453.
| Shark thermoregulation.Crossref | GoogleScholarGoogle Scholar |
Chesson, J. (1978). Measuring preference in selective predation. Ecology 59, 211–215.
| Measuring preference in selective predation.Crossref | GoogleScholarGoogle Scholar |
Claramunt, R. M., Jonas, J. L., Fitzsimons, J. D., and Marsden, J. E. (2005). Influences of spawning habitat characteristics and interstitial predators on lake trout egg deposition and mortality. Transactions of the American Fisheries Society 134, 1048–1057.
| Influences of spawning habitat characteristics and interstitial predators on lake trout egg deposition and mortality.Crossref | GoogleScholarGoogle Scholar |
Cortés, F., Jaureguizar, A. J., Menni, R. C., and Guerrero, R. A. (2011). Ontogenetic habitat preferences of the narrownose smooth-hound shark, Mustelus schmitti, in two Southwestern Atlantic coastal areas. Hydrobiologia 661, 445–456.
| Ontogenetic habitat preferences of the narrownose smooth-hound shark, Mustelus schmitti, in two Southwestern Atlantic coastal areas.Crossref | GoogleScholarGoogle Scholar |
da Silva, C. (2018). Biology, movement behaviour and spatial dynamics of an exploited population of smooth hound shark Mustelus mustelus around a coastal marine protected area in South Africa. Ph.D. Thesis, University of Cape Town, Cape Town, South Africa.
da Silva, C., Kerwath, S. E., Attwood, C. G., Thorstad, E. B., Cowley, P. D., Økland, F., Wilke, C. G., and Næsje, T. F. (2013). Quantifying the degree of protection afforded by a no-take marine reserve on an exploited shark. African Journal of Marine Science 35, 57–66.
| Quantifying the degree of protection afforded by a no-take marine reserve on an exploited shark.Crossref | GoogleScholarGoogle Scholar |
da Silva, C., Attwood, C. G., Wintner, S. P., Wilke, C. G., Winker, H., Smale, M. J., and Kerwath, S. E. (2021). Life history of Mustelus mustelus in the Langebaan Lagoon marine protected area. Marine and Freshwater Research 72, 1142–1159.
| Life history of Mustelus mustelus in the Langebaan Lagoon marine protected area.Crossref | GoogleScholarGoogle Scholar |
Dewitt, C. B., and Friedman, R. M. (1979). Significance of skewness in ectotherm thermoregulation. American Zoologist 19, 195–209.
| Significance of skewness in ectotherm thermoregulation.Crossref | GoogleScholarGoogle Scholar |
DiGirolamo, A. L., Gruber, S. H., Pomory, C., and Bennett, W. A. (2012). Diel temperature patterns of juvenile lemon sharks Negaprion brevirostris, in a shallow-water nursery. Journal of Fish Biology 80, 1436–1448.
| Diel temperature patterns of juvenile lemon sharks Negaprion brevirostris, in a shallow-water nursery.Crossref | GoogleScholarGoogle Scholar | 22497392PubMed |
Dingle, R. D. H. (1996). ‘Migration: the Biology of Life on the Move.’ (Oxford University Press: New York, NY, USA.)
Dingle, H., and Drake, V. A. (2007). What is migration? Bioscience 57, 113–121.
| What is migration?Crossref | GoogleScholarGoogle Scholar |
Economakis, A. E., and Lobel, P. S. (1998). Aggregation behavior of the grey reef shark, Carcharhinus amblyrhynchos, at Johnston Atoll, Central Pacific Ocean. Environmental Biology of Fishes 51, 129–139.
| Aggregation behavior of the grey reef shark, Carcharhinus amblyrhynchos, at Johnston Atoll, Central Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |
Elisio, M., Colonello, J. H., Cortés, F., Jaureguizar, A. J., Somoza, G. M., and Macchi, G. J. (2017). Aggregations and reproductive events of the narrownose smooth-hound shark (Mustelus schmitti) in relation to temperature and depth in coastal waters of the south-western Atlantic Ocean (38–42°S). Marine and Freshwater Research 68, 732–742.
| Aggregations and reproductive events of the narrownose smooth-hound shark (Mustelus schmitti) in relation to temperature and depth in coastal waters of the south-western Atlantic Ocean (38–42°S).Crossref | GoogleScholarGoogle Scholar |
Elisio, M., Awruch, C. A., Massa, A. M., Macchi, G. J., and Somoza, G. M. (2019). Effects of temperature on the reproductive physiology of female elasmobranchs: The case of the narrownose smooth-hound shark (Mustelus schmitti). General and Comparative Endocrinology 284, 113242.
| Effects of temperature on the reproductive physiology of female elasmobranchs: The case of the narrownose smooth-hound shark (Mustelus schmitti).Crossref | GoogleScholarGoogle Scholar | 31400435PubMed |
Espinoza, M., Farrugia, T. J., and Lowe, C. G. (2011). Habitat use, movements and site fidelity of the gray smooth-hound shark (Mustelus californicus Gill 1863) in a newly restored southern California estuary. The Journal of Experimental Biology 401, 63–74.
| Habitat use, movements and site fidelity of the gray smooth-hound shark (Mustelus californicus Gill 1863) in a newly restored southern California estuary.Crossref | GoogleScholarGoogle Scholar |
Finstad, B., Okland, F., Bjorn, P. A., and McKinley, R. S. (2005). Migration of hatchery-reared Atlantic salmon and wild anadromous brown trout post-smolts in a Norwegian fjord system. Journal of Fish Biology 66, 86–96.
| Migration of hatchery-reared Atlantic salmon and wild anadromous brown trout post-smolts in a Norwegian fjord system.Crossref | GoogleScholarGoogle Scholar |
Griffiths, M. H., Wilke, C., Penney, A. J., and Melo, Y. (2002). Life history of the white stumpnose Rhabdosargus globiceps (Pisces: Sparidae) off South Africa. South African Journal of Marine Science 24, 281–300.
| Life history of the white stumpnose Rhabdosargus globiceps (Pisces: Sparidae) off South Africa.Crossref | GoogleScholarGoogle Scholar |
Grubbs, R. D. (2010). Ontogenetic shifts in movements and habitat use. In ‘Sharks and their Relatives II: Biodiversity, Adaptive Physiology, and Conservation’. pp. 319–350. (CRC Press: Boca Raton, FL, USA.)
Gruber, S. H., Nelson, D. R., and Morrissey, J. F. (1988). Patterns of activity and space utilization of lemon sharks, Negaprion brevirostris, in a shallow Bahamian lagoon. Bulletin of Marine Science 43, 61–76.
Hammerschlag, N., Skubel, R., Calich, H., Nelson, E., Shiffman, D. S., Wester, J., MacDonald, C. C., Cain, S., Jennings, L., Enchelmaier, A., and Gallagher, A. J. (2017). Nocturnal and crepuscular behavior in elasmobranchs: A review of movement, habitat use, foraging, and reproduction in the dark. Bulletin of Marine Science 93, 355–374.
Harris, J. E. (1952). A note on the breeding season, sex ratio and embryonic development of the dogfish Scyliorhinus canicula (L.). Journal of the Marine Biological Association of the United Kingdom 31, 269–275.
| A note on the breeding season, sex ratio and embryonic development of the dogfish Scyliorhinus canicula (L.).Crossref | GoogleScholarGoogle Scholar |
Hedger, R. D., Næsje, T. F., Cowley, P. D., Thorstad, E. B., Attwood, C. G., Økland, F., Wilke, C. G., and Kerwath, S. E. (2010). Residency and migratory behaviour by adult Pomatomus saltatrix in a South African coastal embayment. Estuarine, Coastal and Shelf Science 89, 12–20.
| Residency and migratory behaviour by adult Pomatomus saltatrix in a South African coastal embayment.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Dill, L. M., Marshall, G. J., and Buhleier, B. (2002). Habitat use and foraging behavior of tiger sharks (Galeocerdo cuvier) in a seagrass ecosystem. Marine Biology 140, 237–248.
| Habitat use and foraging behavior of tiger sharks (Galeocerdo cuvier) in a seagrass ecosystem.Crossref | GoogleScholarGoogle Scholar |
Hight, B. V., and Lowe, C. G. (2007). Elevated body temperatures of adult female leopard sharks, Triakis semifasciata, while aggregating in shallow nearshore embayments: evidence for behavioral thermoregulation? Journal of Experimental Marine Biology and Ecology 352, 114–128.
| Elevated body temperatures of adult female leopard sharks, Triakis semifasciata, while aggregating in shallow nearshore embayments: evidence for behavioral thermoregulation?Crossref | GoogleScholarGoogle Scholar |
Holland, K. N., Lowe, C. G., Peterson, J. D., and Gill, A. (1992). Tracking coastal sharks with small boats: hammerhead shark pups as a case study. Marine and Freshwater Research 43, 61–66.
| Tracking coastal sharks with small boats: hammerhead shark pups as a case study.Crossref | GoogleScholarGoogle Scholar |
Holland, K. N., Wetherbee, B. M., Peterson, J. D., and Lowe, C. G. (1993). Movements and distribution of hammerhead shark pups on their natal grounds. Copeia 1993, 495–502.
| Movements and distribution of hammerhead shark pups on their natal grounds.Crossref | GoogleScholarGoogle Scholar |
Hopkins, T. E., and Cech, J. J. (2003). The influence of environmental variables on the distribution and abundance of three elasmobranchs in Tomales Bay, California. Environmental Biology of Fishes 66, 279–291.
| The influence of environmental variables on the distribution and abundance of three elasmobranchs in Tomales Bay, California.Crossref | GoogleScholarGoogle Scholar |
Horton, M., Parker, D., Winker, H., Lamberth, S. J., Hutchings, K., and Kerwath, S. E. (2019). Age, growth and per-recruit stock assessment of southern mullet Chelon richardsonii in Saldanha Bay and Langebaan Lagoon, South Africa. African Journal of Marine Science 41, 313–324.
| Age, growth and per-recruit stock assessment of southern mullet Chelon richardsonii in Saldanha Bay and Langebaan Lagoon, South Africa.Crossref | GoogleScholarGoogle Scholar |
Kerwath, S. E., Thorstad, E. B., Naesje, T. F., Cowley, P. D., Okland, F., Wilke, C., and Attwood, C. G. (2009). Crossing invisible boundaries: the effectiveness of the Langebaan lagoon marine protected area as a harvest refuge for a migratory fish species in South Africa. Conservation Biology 23, 653–661.
| Crossing invisible boundaries: the effectiveness of the Langebaan lagoon marine protected area as a harvest refuge for a migratory fish species in South Africa.Crossref | GoogleScholarGoogle Scholar | 19183207PubMed |
Matern, S. A., Cech, J. J., and Hopkins, T. E. (2000). Diel movements of bat rays, Myliobatis californica, in Tomales Bay, California: evidence for behavioral thermoregulation? Environmental Biology of Fishes 58, 173–182.
| Diel movements of bat rays, Myliobatis californica, in Tomales Bay, California: evidence for behavioral thermoregulation?Crossref | GoogleScholarGoogle Scholar |
McKibben, J. N., and Nelson, D. R. (1986). Patterns of movement and grouping of gray reef sharks, Carcharhinus amblyrhynchos, at Enewetak, Marshall Islands. Bulletin of Marine Science 38, 89–110.
Meese, E. N., and Lowe, C. G. (2020). Active acoustic telemetry tracking and tri-axial accelerometers reveal fine-scale movement strategies of a non-obligate ram ventilator. Movement Ecology 8, 8–17.
| Active acoustic telemetry tracking and tri-axial accelerometers reveal fine-scale movement strategies of a non-obligate ram ventilator.Crossref | GoogleScholarGoogle Scholar | 32071719PubMed |
Morrissey, J. F., and Gruber, S. H. (1993a). Habitat selection by juvenile lemon sharks, Negaprion brevirostris. Environmental Biology of Fishes 38, 311–319.
| Habitat selection by juvenile lemon sharks, Negaprion brevirostris.Crossref | GoogleScholarGoogle Scholar |
Morrissey, J. F., and Gruber, S. H. (1993b). Home range of juvenile lemon sharks, Negaprion brevirostris. Copeia 1993, 425–434.
| Home range of juvenile lemon sharks, Negaprion brevirostris.Crossref | GoogleScholarGoogle Scholar |
Nelson, D. R., McKibben, J. N., Strong, W. R., Lowe, C. G., Sisneros, J. A., Shroeder, D. M., and Lavenberg, R. J. (1997). An acoustic tracking of a megamouth shark, Megachasma pelagios: a crepuscular vertigal migrator. Environmental Biology of Fishes 49, 389–399.
| An acoustic tracking of a megamouth shark, Megachasma pelagios: a crepuscular vertigal migrator.Crossref | GoogleScholarGoogle Scholar |
Nosal, A. P., Cartamil, D. C., Long, J. W., Lührmann, M., Wegner, N. C., and Graham, J. B. (2013). Demography and movement patterns of leopard sharks (Triakis semifasciata) aggregating near the head of a submarine canyon along the open coast of southern California, USA. Environmental Biology of Fishes 96, 865–878.
| Demography and movement patterns of leopard sharks (Triakis semifasciata) aggregating near the head of a submarine canyon along the open coast of southern California, USA.Crossref | GoogleScholarGoogle Scholar |
Oddone, M. C., Paesch, L., and Norbis, V. (2005). Reproductive biology and seasonal distribution of Mustelus schmitti (Elasmobranchii: Triakidae) in the Rio de la Plata oceanic front, south-western Atlantic. Journal of the Marine Biological Association of the United Kingdom 85, 1193–1198.
| Reproductive biology and seasonal distribution of Mustelus schmitti (Elasmobranchii: Triakidae) in the Rio de la Plata oceanic front, south-western Atlantic.Crossref | GoogleScholarGoogle Scholar |
Papastamatiou, Y. P., Cartamil, D. P., Lowe, C. G., Meyer, C. G., Wetherbee, B. M., and Holland, K. N. (2011). Scales of orientation, directed walks and movement path structure in sharks. Journal of Animal Ecology 80, 864–874.
| Scales of orientation, directed walks and movement path structure in sharks.Crossref | GoogleScholarGoogle Scholar |
Papastamatiou, Y. P., Watanabe, Y. Y., Bradley, D., Dee, L. E., Weng, K., Lowe, C. G., and Caselle, J. E. (2015). Drivers of daily routines in an ectothermic marine predator: hunt warm, rest warmer? PLoS One 10, e0127807.
| Drivers of daily routines in an ectothermic marine predator: hunt warm, rest warmer?Crossref | GoogleScholarGoogle Scholar | 26061229PubMed |
Papastamatiou, Y. P., Watanabe, Y. Y., Demšar, U., Leos-Barajas, V., Bradley, D., Langrock, R., Weng, K., Lowe, C. G., Friedlander, A. M., and Caselle, J. E. (2018). Activity seascapes highlight central place foraging strategies in marine predators that never stop swimming. Movement Ecology 6, 9–15.
| Activity seascapes highlight central place foraging strategies in marine predators that never stop swimming.Crossref | GoogleScholarGoogle Scholar | 29951206PubMed |
Rountree, R. A., and Able, K. W. (1996). Seasonal abundance, growth, and foraging habits of juvenile smooth dogfish, Mustelus canis, in a New Jersey estuary. Fishery Bulletin 94, 522–534.
Schofield, G., Bishop, C. M., Katselidis, K. A., Dimopoulos, P., Pantis, J. D., and Hays, G. C. (2009). Microhabitat selection by sea turtles in a dynamic thermal marine environment. Journal of Animal Ecology 78, 14–21.
| Microhabitat selection by sea turtles in a dynamic thermal marine environment.Crossref | GoogleScholarGoogle Scholar |
Shannon, L. V., and Stander, G. H. (1977). Physical and chemical characteristics of water in Saldanha Bay and Langebaan Lagoon. Transactions of the Royal Society of South Africa 42, 441–459.
| Physical and chemical characteristics of water in Saldanha Bay and Langebaan Lagoon.Crossref | GoogleScholarGoogle Scholar |
Sims, D. W. (2003). Tractable models for testing theories about natural strategies: foraging behaviour and habitat selection of free-ranging sharks. Journal of Fish Biology 63, 53–73.
| Tractable models for testing theories about natural strategies: foraging behaviour and habitat selection of free-ranging sharks.Crossref | GoogleScholarGoogle Scholar |
Sims, D. W., Wearmouth, V. J., Southall, E. J., Hill, J. M., Moore, P., Rawlinson, K., Hutchinson, N., Budd, G. C., Righton, D., Metcalfe, J. D., and Nash, J. P. (2006). Hunt warm, rest cool: bioenergetic strategy underlying diel vertical migration of a benthic shark. Journal of Animal Ecology 75, 176–190.
| Hunt warm, rest cool: bioenergetic strategy underlying diel vertical migration of a benthic shark.Crossref | GoogleScholarGoogle Scholar |
Sims, D. W., Southall, E. J., Humphries, N. E., Hays, G. C., Bradshaw, C. J., Pitchford, J. W., James, A., Ahmed, M. Z., Brierley, A. S., Hindell, M. A., and Morrit, D. (2008). Scaling laws of marine predator search behaviour. Nature 451, 1098–1102.
| Scaling laws of marine predator search behaviour.Crossref | GoogleScholarGoogle Scholar | 18305542PubMed |
van Niekerk, L., Adams, J. B., James, N. C., Lamberth, S. J., MacKay, C. F., Turpie, J. K., Weerts, S., and Whitfield, A. K. (2020). An estuary ecosystem classification that encompasses biogeography and a high diversity of types in support of protection and management. African Journal of Aquatic Science 45, 199–216.
| An estuary ecosystem classification that encompasses biogeography and a high diversity of types in support of protection and management.Crossref | GoogleScholarGoogle Scholar |
Vaudo, J., and Lowe, C. G. (2006). Movement patterns of the round stingray Urubatis halleri (Cooper) near a thermal outfall. Journal of Fish Biology 68, 1756–1766.
| Movement patterns of the round stingray Urubatis halleri (Cooper) near a thermal outfall.Crossref | GoogleScholarGoogle Scholar |
Wallman, H. L., and Bennett, W. A. (2006). Effects of parturition and feeding on thermal preference of Atlantic stingray, Dasyatis sabina, Lesueur. Environmental Biology of Fishes 75, 259–267.
| Effects of parturition and feeding on thermal preference of Atlantic stingray, Dasyatis sabina, Lesueur.Crossref | GoogleScholarGoogle Scholar |
West, G., and Stevens, J. D. (2001). Archival tagging of school shark, Galeorhinus galeus, in Australia: initial results. Environmental Biology of Fishes 60, 283–298.
| Archival tagging of school shark, Galeorhinus galeus, in Australia: initial results.Crossref | GoogleScholarGoogle Scholar |
Wilson, S. G., Taylor, J. G., and Pearce, A. F. (2001). The seasonal aggregation of whale sharks at Ningaloo Reef, Western Australia: currents, migrations and the El Nino–Southern Oscillation. Environmental Biology of Fishes 61, 1–11.
| The seasonal aggregation of whale sharks at Ningaloo Reef, Western Australia: currents, migrations and the El Nino–Southern Oscillation.Crossref | GoogleScholarGoogle Scholar |
Wood, S. N. (2006). ‘Generalized additive models: an introduction with R.’ (Texts in Statistical Science, Chapman & Hall: Boca Raton, FL, USA.)
Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A., and Smith, G. M. (2009). ‘Mixed Effects Models and Extensions in Ecology with R.’ (Springer: New York, NY, USA.)