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Many Acropora corals at Scott Reef spawn biannually, but most individuals spawn either in autumn or in spring (not in both seasons) and are thus temporally isolated from one another with respect to reproduction10,25. Gametogenesis takes ~ 4 to 6 months in Acropora corals at Scott Reef10. While it is unknown whether gametogenesis occurs at different rates in the different seasons, coral colonies experience different environmental conditions through the gametogenic period, leading up to spawning in the spring and autumn spawning seasons. Gametogenesis occurs through austral winter and early spring prior to the spring spawning (October/November), when water temperatures are cooler and days are shorter. Conversely, gametogenesis occurs through summer prior to the autumn spawning (March/April), when water temperatures are warmest (potentially stressfully warm), the days are longest, and tropical cyclones occur. Both spring and autumn spawning correspond with seasonal minimums in wind speed26,27. Within the thermal tolerance limits of the coral, warmer water temperatures and longer days theoretically increase energy availability for reproductive processes through increased metabolic activity and elevated photosynthesis28,29. Despite the different environmental conditions through gametogenesis, there were no seasonal differences in fecundity and eggs size observed in the biannually spawning Acropora corals studied here. There are several possibilities for the lack of seasonality observed in reproductive output. Firstly, fecundity and egg size varied widely within species, which confounded inferences about whether reproductive output was higher in a particular season. Other studies have similarly reported high variability, particularly in fecundity. Fecundity can vary widely with season22,30 and between years31, but there is also high variation between colonies, within a single colony22, with colony age30 and between colonies at different depths13. Fecundity can also vary in response to stressors13, however, there was no evidence of environmental stress, such as damaging waves from cyclones or heat stress causing coral bleaching32, before or during the period when samples were collected for this study. Adaptive plasticity in egg size (in response to conditions parents are exposed to), is discussed further below. Secondly, Scott Reef is situated in the tropics (14°S) with relatively small seasonal variations in temperature and day length, and has a light regime that is affected by high cloud cover during the summer cyclone season. Water temperatures are 2–4 °C cooler in the winter months leading up to spring spawning than in the summer months prior to autumn spawning. Day length is 1–2 h shorter in winter compared to summer, however summer cyclones and rainfall mean that overall sunshine hours are higher in the winter months. Consequently, there are cooler temperatures with more sunshine hours in the months leading to the spring spawning and warmer temperatures with less sunshine hours in the months leading to the autumn spawning, which may result in comparable available energy for reproduction during both spawning events. Thirdly, seasonal differences in environmental conditions may indeed drive some seasonal differences in energetics, but these could be channeled into other life history processes, such as calcification12,33, rather than fecundity and egg size. Variation in available energy may also affect egg quality rather than size or number. For example, in other invertebrates (greenlip abalone), while the size of the eggs do not increase, the density of protein and lipids increase throughout the spawning season34 and may indicate an increase in the quality over size of the egg. However, a study on the reef-building coral Montipora capitata, reported stable egg quality (lipids and antioxidants) regardless of the environmental conditions the parent colonies were exposed to, although egg sizes were not presented in this work35. The higher polyp fecundity in spring observed in A. microclados may have been an adaptive response to cooler (less favourable) conditions in spring. That is, an increase in parental investment to increase survival in less favourable conditions36. Alternatively, more sunshine hours during winter gametogenesis may have provided additional energy to produce more eggs in this species.
Early work on egg size and number of eggs suggests a simple trade-off model. That is, assuming resources for reproduction are limited, then an increase in gamete size should result in a reduction in the number of gametes37. Correspondingly, earlier studies of different coral species, genera and morphologies reported an inverse relationship between coral egg sizes and the number of eggs (fecundity)21,22,23, also suggesting that energy is channelled to either fewer large eggs or many small eggs19,20. However, in these cases, the reductions in fecundity with egg size among genera were attributed to the differences in polyp morphology (and sometimes reproductive mode i.e. brooder vs spawner). That is, differences in polyp size and structure can also affect egg size and fecundity38,39 independently of energetics. In our between species comparison, we did not see an inverse relationship between egg size and number of eggs (Fig. 3), but there were also no large differences in corallite size for the seven Acropora species studied here (see Supplementary Table S4 for corallite sizes of our species). However, it is important to note that the differences in reproductive mode and morphology (including polyp structure and size) between genera and species, interferes with the egg size versus number of eggs comparison in the context of a trade-off model. In order to determine if there is a trade-off between egg size and number of eggs, we need to look at individuals within a species. That is, do individuals with large eggs have fewer eggs than individuals with smaller eggs of the same species? We have been unable to locate any other dataset providing a within species comparison. Our study demonstrates that there is no direct relationship between egg size and fecundity, within these species of Acropora, and suggests that there is more than just a simple trade-off in resources influencing these measures.
Egg size has been shown to be a phenotypically plastic trait, regulated by the conditions the parent colony is exposed to. For example, a study on the broadcast spawning ascidian, Styela plicata, demonstrated that parents maintained at high densities produced smaller eggs, presumably reflecting the higher sperm concentrations expected at high adult densities, and therefore reduced requirement for a large target40. While the study was unable to measure the number of gametes, and provide an egg size versus number of eggs comparison, it did suggest that egg size is an adaptive plastic response, rather than a simple energetic constraint. Several studies have also reported varying effects of stress on the number and size of eggs. Under temperature stress sufficient to cause bleaching, corals within the same species can produce either fewer eggs (and maintain size) or smaller eggs (and maintain numbers) depending on their zooxanthellae clade and lipid levels15. Corals exposed to elevated nutrients levels also adjusted their reproductive output, with nitrogen reducing both egg size and number of eggs, and phosphorus producing smaller, but more eggs41. Furthermore, when coral colonies are transplanted to different latitudes, they adjust their egg size to be similar to local colonies. A transplant study conducted in Taiwan reported that coral colonies transplanted to higher latitudes and cooler waters, developed larger eggs, similar to local colonies, as an increased investment response to unfavourable conditions36. This phenotypic plasticity may allow for a type of maternal ‘bet-hedging’, where parents increase within clutch variation in offspring phenotype in response to unpredictable environmental conditions42. The results of our study showed high within species natural variability, but this variability was not consistent with the trade-off model. That is, while there may have been both large and small mature eggs within a species, the large eggs did not necessarily correspond with fewer eggs in a polyp. Within species size variation amongst offspring has traditionally been underestimated43, however, since offspring size can affect dispersal potential, producing a range of sizes, could spread offspring through a range of habitats, thereby spreading the risk of reproductive failure44.
It is often assumed that if resources are limited for reproduction, then an increase in egg size should result in a reduction in the number of eggs37. However, there are no datasets directly comparing egg size and number within coral species. We have shown that in seven Acropora coral species this trade-off between size and number did not occur. We also did not see any seasonal differences in these measures. We recorded high natural variability in both mature egg size and fecundity, a factor that should not be overlooked when using these measures to gauge or compare reproductive output (e.g. between seasons, years, locations). Since egg size and fecundity are affected by parent colony energy reserves, energy allocation to a range of other life history processes (e.g. growth and repair), polyp size and morphology, responses to environmental conditions, and the interaction of these factors, it is unlikely that there is a simple trade-off between size and number of eggs. It is also unlikely that these measures are constrained only by energetics, given the adaptive phenotypic plasticity reported in other studies36, 40. Furthermore, parental investment can come in the form of increased egg quality (e.g. lipids or antioxidants), rather than size or number of eggs. More research into coral energetics, natural variability, and adaptive plasticity is required to determine the mechanisms behind some of the patterns we observed, but our study doesn’t support a simple trade-off model in coral reproduction. More

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The Aedes aegypti mosquito’s taste for human blood has been linked to exposure to dense settlements dotted with sources of water. Credit: Getty

Ecology
23 July 2020

Population density and water storage created a new ecological niche for the disease-carrying insects.

As humans crowd into cities where standing water abounds, even in the driest months, we become an ever-more-tempting target for bloodsuckers.
Only a few of the more than 3,000 species of mosquito specifically seek out blood from humans — but those few are enough to spread diseases that affect some 100 million people every year. To shed light on the evolutionary origin of insects’ taste for humans, Lindy McBride and Noah Rose at Princeton University in New Jersey and their colleagues captured Aedes aegypti mosquitoes at 27 sites across the insects’ ancestral range in sub-Saharan Africa.
The researchers placed hungry females in boxes with two exits: one offering the smell of a human and the other the smell of either a living guinea pig (Cavia porcellus) or a button quail (Coturnix coturnix). Compared with mosquitoes that were indifferent to human blood, those that sought it out were more likely to hail from areas with dense human populations and long, hot, dry seasons.
The researchers suspect that water stored by humans has become a key breeding location in a landscape with little standing water. Their genetic analysis suggests that the taste for humans evolved just once. More

Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada
M. Aaron MacNeil & Taylor Gorham

Institute of Environment, Department of Biological Sciences, Florida International University, North Miami, FL, USA
Demian D. Chapman, Michael Heithaus, Jeremy Kiszka, Mark E. Bond, Kathryn I. Flowers, Gina Clementi, Khadeeja Ali, Laura García Barcia, Erika Bonnema, Camila Cáceres, Naomi F. Farabough, Virginia Fourqurean, Kirk Gastrich, Devanshi Kasana, Yannis P. Papastamatiou, Jessica Quinlan, Maurits van Zinnicq Bergmann & Elizabeth Whitman

Australian Institute of Marine Science, Townsville, Queensland, Australia
Michelle Heupel & Leanne M. Currey-Randall

Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, Queensland, Australia
Colin A. Simpfendorfer, C. Samantha Sherman, Stacy Bierwagen, Brooke D’Alberto, Lachlan George, Sushmita Mukherji & Audrey Schlaff

Australian Institute of Marine Science, Crawley, Western Australia, Australia
Mark Meekan, Conrad W. Speed, Matthew J. Rees & Dianne McLean

The UWA Oceans Institute, The University of Western Australia, Crawley, Western Australia, Australia
Mark Meekan, Conrad W. Speed & Dianne McLean

School of Molecular and Life Sciences, Curtin University, Bentley, Western Australia, Australia
Euan Harvey & Jordan Goetze

Marine Program, Wildlife Conservation Society, New York, NY, USA
Jordan Goetze

Centre for Sustainable Ecosystems Solutions, School of Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, New South Wales, Australia
Matthew J. Rees

Australian Institute of Marine Science, Arafura Timor Research Facility, Darwin, Northern Territory, Australia
Vinay Udyawer

School of Marine and Atmospheric Science, Stony Brook University, Stony Brook, NY, USA
Jasmine Valentin-Albanese, Diego Cardeñosa, Stephen Heck & Bradley Peterson

International Pole and Line Foundation, Malé, Maldives
M. Shiham Adam

Maldives Marine Research Institute, Ministry of Fisheries, Marine Resources and Agriculture, Malé, Maldives
Khadeeja Ali

Centro de Investigaciones de Ecosistemas Costeros (CIEC), Cayo Coco, Morón, Ciego de Ávila, Cuba
Fabián Pina-Amargós

Centro de Investigaciones Marinas, Universidad de la Habana, Havana, Cuba
Jorge A. Angulo-Valdés & Alexei Ruiz-Abierno

Galbraith Marine Science Laboratory, Eckerd College, St Petersburg, FL, USA
Jorge A. Angulo-Valdés

Joint Institute for Marine and Atmospheric Research, University of Hawaii at Manoa, Honolulu, HI, USA
Jacob Asher

Habitat and Living Marine Resources Program, Ecosystem Sciences Division, Pacific Islands Fisheries Science Center, National Oceanic and Atmospheric Administration, Honolulu, HI, USA
Jacob Asher

Réseau requins des Antilles Francaises, Kap Natirel, Vieux-Fort, Guadeloupe
Océane Beaufort

Mahonia Na Dari Research and Conservation Centre, Kimbe, Papua New Guinea
Cecilie Benjamin

South African Institute for Aquatic Biodiversity, Grahamstown, South Africa
Anthony T. F. Bernard

Department of Zoology and Entomology, Rhodes University, Grahamstown, South Africa
Anthony T. F. Bernard

Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
Michael L. Berumen, Jesse E. M. Cochran & Royale S. Hardenstine

Blue Resources Trust, Colombo, Sri Lanka
Rosalind M. K. Bown, Daniel Fernando, Nishan Perera & Akshay Tanna

Bren School of Environmental Sciences and Management, University of California Santa Barbara, Santa Barbara, CA, USA
Darcey Bradley

Shark Research and Conservation Program, Cape Eleuthera Institute, Cape Eleuthera, Eleuthera, Bahamas
Edd Brooks

Center for Sustainable Development, College of Arts and Sciences, Qatar University, Doha, Qatar
J. Jed Brown

University of the West Indies, Discovery Bay Marine Laboratory, Discovery Bay, Jamaica
Dayne Buddo

Department of Biological Sciences, Macquarie University, Sydney, New South Wales, Australia
Patrick Burke

Albion College, Albion, MI, USA
Jeffrey C. Carrier

Marine Science Institute, University of California Santa Barbara, Santa Barbara, CA, USA
Jennifer E. Caselle

Coastal Impact, Quitula, Aldona Bardez, India
Venkatesh Charloo

CUFR Mayotte & Marine Biodiversity, Exploitation and Conservation (MARBEC), Université de Montpellier, CNRS, IRD, IFREMER, Montpellier, France
Thomas Claverie

PSL Research University, LABEX CORAIL, CRIOBE USR3278 EPHE-CNRS-UPVD, Mòorea, French Polynesia
Eric Clua

Environmental Research Institute Charlotteville, Charlotteville, Trinidad and Tobago
Neil Cook, Lanya Fanovich & Aljoscha Wothke

School of Biosciences, Cardiff University, Cardiff, UK
Neil Cook

ARC Centre of Excellence in Coral Reef Studies, James Cook University, Townsville, Queensland, Australia
Jessica Cramp & Joshua E. Cinner

Sharks Pacific, Rarotonga, Cook Islands
Jessica Cramp

Wageningen Marine Research, Wageningen University & Research, IJmuiden, The Netherlands
Martin de Graaf

Graduate School of Global Environmental Studies, Sophia University, Tokyo, Japan
Mareike Dornhege

Waitt Institute, La Jolla, CA, USA
Andy Estep

Marine Megafauna Foundation, Truckee, CA, USA
Anna L. Flam, Andrea Marshall & Alexandra M. Watts

The South African Association for Marine Biological Research, Oceanographic Research Institute, Durban, South Africa
Camilla Floros

Departamento de Botânica e Zoologia, Universidade Federal do Rio Grande do Norte, Natal, Brazil
Ricardo Garla

Independent consultant, Hull, UK
Rory Graham

Bimini Biological Field Station Foundation, South Bimini, Bahamas
Tristan Guttridge & Maurits van Zinnicq Bergmann

Saving the Blue, Kendall, Miami, FL, USA
Tristan Guttridge

Biology Department, College of Science, UAE University, Al Ain, United Arab Emirates
Aaron C. Henderson

The School for Field Studies Center for Marine Resource Studies, South Caicos, Turks and Caicos Islands
Aaron C. Henderson & Heidi Hertler

Center for Shark Research, Mote Marine Laboratory, Sarasota, FL, USA
Robert Hueter

Operation Wallacea, Spilsby, Lincolnshire, UK
Mohini Johnson

Wildlife Conservation Society, Melanesia Program, Suva, Fiji
Stacy Jupiter

Daniel P. Haerther Center for Conservation and Research, John G. Shedd Aquarium, Chicago, IL, USA
Steven T. Kessel

Kenya Fisheries Service, Mombasa, Kenya
Benedict Kiilu

Ministry of Fisheries and Marine Resources, Development, Kiritimati, Kiribati
Taratu Kirata

Tanzania Fisheries Research Institute, Dar Es Salaam, Tanzania
Baraka Kuguru

University of the West Indies, Kingston, Jamaica
Fabian Kyne

School of Biological Sciences, The University of Western Australia, Perth, Western Australia, Australia
Tim Langlois

Fish Ecology and Conservation Physiology Laboratory, Carleton University, Ottawa, Ontario, Canada
Elodie J. I. Lédée

Coral Reef Research Foundation, Koror, Palau
Steve Lindfield

Departamento de Ecología y Territorio, Facultad de Estudios Ambientales y Rurales, Pontificia Universidad Javeriana, Bogotá, Colombia
Andrea Luna-Acosta

National Institute of Water and Atmospheric Research, Hataitai, New Zealand
Jade Maggs

Endangered Marine Species Research Unit, Borneo Marine Research Institute, Universiti Malaysia Sabah, Kota Kinabalu, Malaysia
B. Mabel Manjaji-Matsumoto

Department of Marine Biology, Texas A&M University at Galveston, Galveston, TX, USA
Philip Matich

Aquarium of the Pacific, Long Beach, CA, USA
Erin McCombs

Khaled bin Sultan Living Oceans Foundation, Annapolis, MD, USA
Llewelyn Meggs

Department of Biodiversity, Conservation & Attractions, Parks & Wildlife WA, Pilbara Region, Nickol, Western Australia, Australia
Stephen Moore

Large Marine Vertebrates Research Institute Philippines, Jagna, The Philippines
Ryan Murray & Alessandro Ponzo

Wasage Divers, Wakatobi and Buton, Indonesia
Muslimin Kaimuddin

Western Australian Fisheries and Marine Research Laboratories, Department of Primary Industries and Regional Development, Government of Western Australia, North Beach, Western Australia, Australia
Stephen J. Newman & Michael J. Travers

Island Conservation Society Seychelles, Victoria, Mahé, Seychelles
Josep Nogués

CORDIO East Africa, Mombasa, Kenya
Clay Obota & Melita Samoilys

The Centre for Ocean Research and Education, Gregory Town, Eleuthera, Bahamas
Owen O’Shea

Department of Environment and Geography, University of York, York, UK
Kennedy Osuka

Center for Fisheries Research, Ministry for Marine Affairs and Fisheries, Jakarta Utara, Indonesia
Andhika Prasetyo

Universitas Dayanu Ikhsanuddin Bau-Bau, Bau-Bau, Indonesia
L. M. Sjamsul Quamar

Pristine Seas, National Geographic Society, Washington, DC, USA
Enric Sala

Department of Zoology, University of Oxford, Oxford, UK
Melita Samoilys

HJR Reefscaping, Boquerón, Puerto Rico
Michelle Schärer-Umpierre

SalvageBlue, Kingstown, Saint Vincent and the Grenadines
Nikola Simpson

School of Natural and Computational Sciences, Massey University, Auckland, New Zealand
Adam N. H. Smith

Indo Ocean Project, PT Nomads Diving Bali, Nusa Penida, Indonesia
Lauren Sparks

Manchester Metropolitan University, Manchester, UK
Akshay Tanna & Alexandra M. Watts

Reef Check Dominican Republic, Santo Domingo, Dominican Republic
Rubén Torres

Institut de Recherche pour le Développement, UMR ENTROPIE (IRD-UR-UNC-CNRS-IFREMER), Nouméa, New Caledonia
Laurent Vigliola

Secretariat of the Pacific Regional, Environment Programme, Apia, Samoa
Juney Ward

Department of Life Science, Tunghai University, Taichung, Taiwan
Colin Wen

School of Environmental and Forest Sciences, University of Washington, Seattle, WA, USA
Aaron J. Wirsing

Corales del Rosario and San Bernardo National Natural Park, GIBEAM Research Group, Universidad del Sinú, Cartagena, Colombia
Esteban Zarza-Gonzâlez

D. Chapman and M. Heithaus conceived the study with assistance from M. Heupel, C.A.S., M.M., E.H. and M.A.M. D. Chapman, M. Heithaus, M. Heupel, C.A.S., M.M. and E.H. directed fieldwork run by J.G., J.K., M.E.B., L.M.C.-R., C.W.S., K.I.F., J.V.-A., G.C. and C.S.S. Database management was by T. Gorham. M.A.M. and D. Chapman drafted the manuscript, with help from M. Heithaus, M. Heupel, C.A.S., J.E.M.C., M.M., E.H., J.G., J.K., M.E.B., L.M.C.-R., C.W.S., C.S.S., M.J.R., V.U. and T. Gorham. All other authors contributed equally, made substantial contributions to data collection, provided input and approved the text in the manuscript. More

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