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    1H NMR based metabolic profiling distinguishes the differential impact of capture techniques on wild bighorn sheep

    Examining the serum metabolome profiles of bighorn sheep captured by the three primary techniques used to capture wild ungulates revealed significant changes in polar metabolite levels between the different animal groups, and trends that persisted throughout the analyses when directly comparing, in a pairwise fashion, specific capture techniques. Results from PLS-DA modeling and analysis of the top 15 metabolites that contribute most (VIP  > 1.2) to the separation of the three capture groups revealed that amino acid levels of tryptophan, valine, isoleucine, phenylalanine, and proline were highest in animals captured by dart, with intermediate levels in animals capture using dropnets, and lowest in animals captured using the helicopter method (Fig. 3A). One-way ANOVA analyses identified additional amino acids that displayed similar decreasing level trends from dart to dropnet to helicopter capture (dart  > drop net  > helicopter) methods, and included arginine, asparagine, aspartate, cysteine, glutamate, and glutamine, glycine, histidine, leucine, lysine, serine, and tyrosine (Fig. 4). These metabolite level changes suggest a shift in amino acid metabolism, and a potentially higher catabolism of these compounds as a function of increasingly more energetically intense and possibly more stressful capture methods such as helicopter capture.Of these amino acids, aspartate, glycine, and glutamate function as precursors for neurotransmitter synthesis, and may therefore be valuable indicators of the capture techniques’ impacts on animal health and changes to their physiological state. Glutamate is a fundamental component of nitrogen excretion in the urea cycle, and its lower serum levels in animals captured by helicopter support the idea of altered metabolite flow through the urea cycle. In addition to these patterns, decreasing levels of aspartate were observed in samples of dropnet and helicopter captured animals compared to the levels found in the dart-captured animals. The change regarding urea cycle alterations also manifested itself in differential serum urea levels, with fold changes (FC) between the groups decreasing significantly with capture techniques, with a mean FC difference of 1.4 for the dart-captured group, 0.26 for the dropnet-captured group, and − 0.3 for the helicopter-captured animals (Supplementary Table S2). As urea recycling is a prominent feature of ruminant metabolism and urea flux can rapidly change, the urea concentration changes observed between the three capture techniques support an impact on urea cycle intermediates29. While the trend of an overall decrease in urea cycle intermediates parallels a similar trend in amino acid concentrations, the extent to which amino acid metabolism is linked to changes in urea cycle activity is difficult to evaluate due to the nature of nitrogen recycling in the rumen of these ruminants.Other metabolites found in significantly higher concentrations in the serum samples of dart-captured animals compared to the two other techniques included: formate, glucose, 3-hydroxybutyrate, dimethylamine, carnitine (Fig. 3A). Propionate, which was observed to be higher in the dart and dropnet captured animals than that of helicopter captured animals (Fig. 4) is of interest, as it is the main precursor for glucose synthesis in the liver of ruminants30, and potentially reflect a higher dependence of ruminants on gluconeogenesis due to the almost complete conversion of available dietary carbohydrates to volatile fatty acids in the rumen31. As animal capture via nets increases physical activity as the animals struggle to free themselves from entanglement, generally resulting in longer times animals are under physical restraint, as well as the increased physical exertion and stress as they attempt to flee the pursuing helicopter, the observed decrease in serum propionate levels may reflect increased needs to generate glucose de novo via gluconeogenesis.This interpretation of the metabolite data is reinforced by the observation of significantly elevated levels of O-acetylcarnitine in the drop net and helicopter net gun animal capture groups compared to the darted animals (Fig. 4). As an important element of the carnitine/acyl-carnitine shuttle and import of fatty acids into the mitochondria for β-oxidation, acyl-carnitine is a major contributor to the flow of acyl groups into the TCA cycle, and a robust indicator of cardiac output and, by extension, TCA cycle activity levels in mammals32. Additional metabolites that displayed distinctly increasing trends based on capture method (dart  More

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    Ixodiphagus hookeri wasps (Hymenoptera: Encyrtidae) in two sympatric tick species Ixodes ricinus and Haemaphysalis concinna (Ixodida: Ixodidae) in the Slovak Karst (Slovakia): ecological and biological considerations

    1.George, J. E., Pound, J. M. & Davey, R. B. Chemical control of ticks on cattle and the resistance of these parasites to acaricides. Parasitology 129(S1), 5353–5366 (2004).Article 
    CAS 

    Google Scholar 
    2.Abbas, R. Z. et al. Acaricide resistance in cattle ticks and approaches to its management: The state of play. Vet. Parasitol. 203, 6–20 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    3.Yessinou, R. E. et al. Resistance of tick Rhipicephalus microplus to acaricides and control strategies. J. Ent. Zool. Stud. 4, 408–414 (2016).
    Google Scholar 
    4.Bradberry, S. M. et al. Poisoning due to pyrethroids. Toxicol. Rev. 24, 93–106 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    5.Klainbart, S. et al. Tremor salivation syndrome in canine following pyrethroid/permethrin intoxication. Pharm. Anal. Acta 5, 320 (2014).
    Google Scholar 
    6.Antwi, F. B. & Reddy, G. V. P. Toxicological effects of pyrethroids on non-target aquatic insects. Environ. Toxicol. Pharmacol. 40, 915–923 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    7.Glorennec, P. et al. Determinants of children’s exposure to pyrethroid insecticides in western France. Environ. Int. 104, 76–82 (2017).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    8.Alfeev, N. I. The utilization of Hunterellus hookeri How. for the control of the ticks, Ixodes ricinus L. and Ixodes persulcatus P. Sch. with reference to peculiarities of their metamorphosis under conditions of the Province of Lenningrad. Rev. Appl. Ent. B. 34, 108–109 (1946).
    Google Scholar 
    9.Hu, R., Hyland, K. E. & Oliver, J. H. A review on the use of Ixodiphagus wasps (Hymenoptera: Encyrtidae) as natural enemies for the control of ticks (Acari: Ixodidae). Syst. Appl. Acarol. 3, 19–28 (1988).
    Google Scholar 
    10.Mwangi, E. N. et al. The impact of Ixodiphagus hookeri, a tick parasitoid, on Amblyomma variegatum (Acari: Ixodidae) in a field trial in Kenya. Exp. Appl. Acarol. 21, 117–126 (1997).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    11.Takasu, K. & Nakamura, S. Life history of the tick parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae) in Kenya. Biol. Control 46, 114–121 (2008).Article 

    Google Scholar 
    12.Rehacek, J. & Kocianova, E. Attempt to infect Hunterellus hookeri Howard (Hymenoptera, Encyrtidae), an endoparasite of ticks, with Coxiella burnetti. Acta Virol. 36, 492 (1992).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    13.Plantard, O. et al. Detection of Wolbachia in the tick Ixodes ricinus is due to the presence of the hymenoptera endoparasitoid Ixodiphagus hookeri. PLoS ONE 7, e30692 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    14.Bohacsova, M. et al. Arsenophonus nasoniae and Rickettsiae infection of Ixodes ricinus due to parasitic wasp Ixodiphagus hookeri. PLoS ONE 11, e0149950 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    15.Mather, T. N., Piesman, J. & Spielman, A. Absence of spirochete (Borrelia burgdorferi) and piroplasms (Babesia microti) in deer tick (Ixodes dammini) parasitized by Chalcid wasps (Hunterellus hookeri). Med. Vet. Entomol. 1, 3–8 (1987).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Noda, H., Munderloh, U. & Kurtti, T. Endosymbionts of ticks relationship to Wolbachia spp. and tick-borne pathogens of humans and animals. Appl. Environ. Microbiol. 63, 3926–3932 (1997).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.Ahantarig, A. et al. Hard ticks and their bacterial endosymbionts (or would be pathogens). Folia Microbiol. 58, 419–428 (2013).CAS 
    Article 

    Google Scholar 
    18.Duron, O. et al. Evolutionary changes in symbiont community structure in ticks. Mol. Ecol. 26, 2905–2921 (2017).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    19.Vila, A. et al. Endosymbionts carried by ticks feeding on dogs in Spain. Ticks Tick Borne Dis. 10, 848–852 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Cooley, R. A. & Kohls, G. M. A summary of tick parasites. In Proceedings of the 5th Pacific Science Congress, Vol. 5, 3375–3381 (1934).21.Bowman, J. L., Logan, T. M. & Hair, J. A. Host suitability of Ixodiphagus texanus Howard on five species of hard ticks. J. Agric. Entomol. 3, 1–9 (1986).
    Google Scholar 
    22.Mather, T. N., Piesman, J. & Spielman, A. Absence of spirochete (Borrelia burgdorferi ) and piroplasms (Babesia microti) in deer tick (Ixodes dammini) parasitized by Chalcid wasps (Hunterellus hookeri). Med. Vet. Entomol. 1, 3–8 (1987).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Hu, R., Hyland, K. E. & Mather, T. N. Occurrence and distribution in Rhode Island of Hunterellus hookeri (Hymenoptera: Encyrtidae), a wasp parasitoid of Ixodes dammini. J. Med. Entomol. 30, 277–280 (1993).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Stafford, K. C. 3rd., Denicola, A. J. & Kilpatrick, H. J. Reduced abundance of Ixodes scapularis (Acari: Ixodidae) and the tick parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae) with reduction of white-tailed deer. J. Med. Entomol. 40, 642–652 (2003).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    25.Hu, R. & Hyland, K. E. Prevalence and seasonal activity of the wasp parasitoid, Ixodiphagus hookeri (Hymenoptera: Encyrtidae) in its tick host, Ixodes scapularis (Acari: Ixodidae). Syst. Appl. Acarol. 2, 95–100 (1997).
    Google Scholar 
    26.Lopes, A. J. O. et al. Parasitism by Ixodiphagus Wasps (Hymenoptera: Encyrtidae) in Rhipicephalus sanguineus and Amblyomma Ticks (Acari: Ixodidae) in Three Regions of Brazil. J. Econ. Entomol. 5, 1979–1981 (2012).Article 

    Google Scholar 
    27.Fiedler, O. G. H. A new African tick parasite, Hunterellus theilerae sp. n. Onderstepoort. J. Vet. Res. 26, 61–63 (1953).
    Google Scholar 
    28.Hoogstraal, H. & Kaiser, M. N. Records of Hunterellus theileri Fielder (Encyrtidae: Chalcidoidea) parasitizing Hyalomma ticks on birds migrating through Egypt. Ann. Ent. Soc. Am. 54, 616–617 (1961).Article 

    Google Scholar 
    29.Mwangi, E. N., Newson, R. M. & Kaaya, G. P. A hymenopteran parasitoid of the Bont tick Amblyomma variegatum Fabricius (Acarina: Ixodidae) in Kenya. Discov. Innov. 5, 331–335 (1993).
    Google Scholar 
    30.Shastri, U. V. Some observations on Hunterellus hookeri Howard, a parasitoid of Hyalomma-anatolicum anatolicum Koch, 1844 in Marathwada region Maharashtra State. Cheiron 13, 67–71 (1984).
    Google Scholar 
    31.Gaye, M. et al. Hymenopteran parasitoids of hard ticks in western Africa and the Russian Far East. Microorganisms 8, 1992 (2020).CAS 
    PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    32.Oliver, J. H. A wasp parasite of the possum tick, Ixodes tasmani, Australia. Pan-Pac. Entomol. 40, 227–230 (1964).
    Google Scholar 
    33.Doube, B. M. & Heath, A. C. G. Observations on the biology and seasonal abundance of an encyrtid wasp, a parasite of ticks in Queensland. J. Med. Entomol. 12, 433–447 (1975).CAS 
    PubMed 

    Google Scholar 
    34.Heath, A. C. G. & Cane, R. P. A new species of Ixodiphagus (Hymenoptera: Chalcidoidea: Encyrtidae) parasitizing seabird ticks in New Zealand. N. Z. J. Zool. 37, 147–155 (2010).Article 

    Google Scholar 
    35.Costa Lima, A. The chalcid Hunterellus hookeri Howard, a parasite of the tick Rhipicephalus sanguineus Latreille, observed in Rio de Janeiro. Rev. Vet. Zoot. 5, 201–203 (1915).
    Google Scholar 
    36.Philip, C. B. Occurrence of a colony of the tick parasite Hunterellus hookeri Howard in West Africa. US Public Health Serv. Rpts. 46, 2168–2172 (1931).Article 

    Google Scholar 
    37.Bishopp, F. C. Record of hymenopterous parasites of ticks in the United States. Proc. Entomol. Soc. Wash. 36, 87–88 (1934).
    Google Scholar 
    38.Gahan, A. B. On the identities of chalcidoid tick parasites (Hymenoptera). Proc. Entomol. Soc. Wash. 36, 89–97 (1934).
    Google Scholar 
    39.Munaf, H. B. The first record of Hunterellus hookeri parasitizing Rhipicephalus sanguineus in Indonesia. South Asian J. Tropic. Med. Public Health 7, 492 (1976).CAS 

    Google Scholar 
    40.Cheong, W. H., Rajamanikam, C. & Mahadevan, S. A case of Hunterellus hookeri parasitization of ticks in Pentaling Jaya, Peninsula Malaysia. South Asian J. Tropic. Med. Publ. Health 9, 456–458 (1978).CAS 

    Google Scholar 
    41.Coronado, A. Ixodiphagus hookeri Howard, 1907 (Hymenoptera: Encyrtidae) in the brown dog tick Rhipicephalus sanguineus Latreille, 1806 (Acari: Ixodidae) in Venezuela. Entomotropica 21, 61–64 (2006).
    Google Scholar 
    42.Bezerra Santos, M. et al. Larvae of Ixodiphagus wasps (Hymenoptera: Encyrtidae) in Rhipicephalus sanguineus sensu lato ticks (Acari: Ixodidae) from Brazil. Ticks Tick Borne Dis. https://doi.org/10.1016/j.ttbdis.2017.03.004 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    43.Řehaček, J. Uzitočný cudzopasnik. Enviromagazin 3, 19 (1998).
    Google Scholar 
    44.Collatz, J. et al. A hidden beneficial: Biology of the tick-wasp Ixodiphagus hookeri in Germany. J. Appl. Entomol. 135, 351–358 (2011).Article 

    Google Scholar 
    45.Tijsse-Klasen, E. et al. Parasites of vectors—Ixodiphagus hookeri and its Wolbachia symbionts in ticks in the Netherlands. Parasit. Vectors 4, 228 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Ramos, R. A. et al. Occurrence of Ixodiphagus hookeri (Hymenoptera: Encyrtidae) in Ixodes ricinus (Acari: Ixodidae) in southern Italy. Ticks Tick Borne Dis. 6, 234–236 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    47.Sormunen, J. J. et al. First evidence of Ixodiphagus hookeri (Hymenoptera: Encyrtidae) parasitization in Finnish castor bean ticks (Ixodes ricinus). Exp. Appl. Acarol. 79, 395–404 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    48.Krawczyk, A. I. et al. Tripartite interactions among Ixodiphagus hookeri, Ixodes ricinus and deer: Differential interference with transmission cycles of tick-borne pathogens. Pathogens 9, 339 (2020).PubMed Central 
    Article 

    Google Scholar 
    49.Pervomaisky, G. S. On the infestation of Ixodes persulcatus by Hunterellus hookeri How. (Hymenoptera). Zool. Zh. 22, 211–213 (1943).
    Google Scholar 
    50.Alfeev, N. I. & Klimas, Y. V. Experience in cultivating ichneumon flies, Hunterellus hookeri, obtained from United States, which destroy ixodid ticks of Soviet fauna. Priroda 2, 98–101 (1938).
    Google Scholar 
    51.Brumpt, E. Utilisation des insectes auxiliares entomophages dans la lutte contre les insectes pathogenes. Presse Med. Paris 36, 359–361 (1913).
    Google Scholar 
    52.Klyushkina, E. A. A parasite of the ixodid ticks, Hunterellus hookeri How. in the Crimea. Zool. Zh. 37, 1561–1563 (1958).
    Google Scholar 
    53.Slovak, M. Finding of the endoparasitoid Ixodiphagus hookeri (Hymenoptera, Encyrtidae) in Haemaphysalis concinna ticks in Slovakia. Biologia 58, 890 (2003).
    Google Scholar 
    54.Brumpt, E. Parasitisme latent de l’Ixodiphagus caucurtei chez les larves gorgées et les nymphes á jeun de divers ixodines (Ixodes ricinus et Rhipicephalus sanguineus). Comptes Rendus de l’Académie des Sciences de Paris 191, 1085–1087 (1930).
    Google Scholar 
    55.Boucek, Z. & Černy, V. A parasite of ticks, the chalcid Hunterellus hookeri in Czechoslovakia. Zool. Listy 3, 109–111 (1954).
    Google Scholar 
    56.Heglasová, I. et al. Ticks, fleas and rodent-hosts analyzed for the presence of Borrelia miyamotoi in Slovakia: The first record of Borrelia miyamotoi in a Haemaphysalis inermis tick. Ticks Tick Borne Dis. 11, 101456 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    57.Nosek, J. The ecology, bionomics and behavior of Haemaphysalis (Haemaphysalis) concinna tick. Z. Parasitenkd. 36, 233–241 (1971).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    58.Nosek, J. The ecology and public health importance of Dermacentor marginatus and D. reticulatus ticks in central Europe. Folia Parasitol. 19, 93–102 (1972).CAS 

    Google Scholar 
    59.Széll, Z. et al. Temporal distribution of Ixodes ricinus, Dermacentor reticulatus and Haemaphysalis concinna in Hungary. Vet. Parasitol. 141, 377–379 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    60.Harnok, S. & Farkas, R. Influence of biotope on the distribution and peak activity of questing ixodid ticks in Hungary. Med. Vet. Entomol. 23, 41–46 (2009).Article 

    Google Scholar 
    61.Bartosik, K., Wiśniowski, L. & Buczek, A. Abundance and seasonal activity of adult Dermacentor reticulatus (Acari: Amblyommidae) in eastern Poland in relation to meteorological conditions and the photoperiod. Ann. Agric. Environ. Med. 18, 340–344 (2011).PubMed 
    PubMed Central 

    Google Scholar 
    62.Egyed, L. et al. Seasonal activity and tick-borne pathogen infection rates of Ixodes ricinus ticks in Hungary. Ticks Tick Borne Dis. 3, 90–94 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Hornok, S. et al. Ixodid ticks on ruminants, with on-host initiated moulting (apolysis) of Ixodes, Haemaphysalis and Dermacentor larvae. Vet. Parasitol. 187, 350–353 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    64.Buczek, A. et al. Threat of attacks of Ixodes ricinus ticks (Ixodida: Ixodidae) and Lyme borreliosis within urban heat islands in south-western Poland. Parasit. Vectors 7, 562 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    65.Chitimia-Dobler, L. Spatial distribution of Dermacentor reticulatus in Romania. Vet. Parasitol. 214, 219–223 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    66.Pfäffle, M., Littwin, N. & Petney, T. Host preferences of immature Dermacentor reticulatus (Acari: Ixodidae) in a forest habitat in Germany. Ticks Tick Borne Dis. 6, 508–515 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    67.Collatz, J. et al. Being a parasitoid of parasites: Host finding in the tick wasp Ixodiphagus hookeri by odours from mammals. Ent. Exp. Appl. 134, 131–137 (2010).Article 

    Google Scholar 
    68.Takasu, K. et al. Host recognition by the tick parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae). Environ. Entomol. 32, 614–617 (2003).Article 

    Google Scholar 
    69.Demas, F. A. et al. Cattle and Amblyomma variegatum odors used in host habitat and host finding by the tick parasitoid, Ixodiphagus hookeri. J. Chem. Ecol. 26, 1079–1093 (2000).CAS 
    Article 

    Google Scholar 
    70.Alfeev, N. I. & Klimas, Y. V. On the possibility of developing ichneumon flies, Hunterellus hookeri in climatic conditions of the USSR. Sovet. Vet. 15, 55 (1938).
    Google Scholar 
    71.Logan, T. M., Bowman, J. L. & Hair, J. A. Parthenogenesis and overwintering behavior in Ixodiphagus texanus Howard. J. Agric. Entomol. 2, 272–276 (1985).
    Google Scholar 
    72.Wood, H. P. Notes on the life history of the tick parasite Hunterellus hookeri Howard. J. Econ. Entomol. 4, 425–431 (1911).Article 

    Google Scholar 
    73.Cooley, R. A. & Kohls, G. M. Egg laying of Ixodiphagus caucurtei du Buysson in larval ticks. Science 67, 656 (1928).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    74.Hu, R. Identification of the wasp parasitoid of the deer tick, Ixodes dammini, in Rhode Island and its implication in the control of Lyme disease. M.S. thesis, University of Rhode Island, USA (1990).75.Mwangi, E. N. et al. Parasitism of Amblyomma variegatum by a hymenopteran parasitoid in the laboratory, and some aspects of its basic biology. Biol. Control 4, 101–104 (1994).Article 

    Google Scholar 
    76.Hu, R. & Hyland, K. E. Effects of the feeding proces of Ixodes scapularis (Acari: Ixodidae) on embryonic development of its parasitoid, Ixodiphagus hookeri (Hymenoptera: Encyrtidae). J. Med. Entomol. 35, 1050–1053 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    77.Knipling, E. F. & Steelman, C. D. Feasibility of controlling Ixodes scapularis ticks (Acari: Ixodidae), the vector of Lyme disease, by parasitoid augmentation. J. Med. Entomol. 37, 647–652 (2000).Article 

    Google Scholar 
    78.Stafford, K. C. 3rd., Denicola, A. J. & Magnarelli, L. A. Presence of Ixodiphagus hookeri (Hymenoptera: Encyrtidae) in two Connecticut populations of Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 33, 183–188 (1996).PubMed 
    Article 

    Google Scholar 
    79.Cole, M. M. Biological control of ticks by the use of hymenopterous insects. A review. World Health Organization (WHO/EBL/43.66) 43, 1–12 (1965).
    Google Scholar 
    80.Hoogstraal, H., Santana, F. J. & van Peenen, P. F. D. Ticks (Ixodoidea) of Mt. Sontra, Danang, Republic of Vietnam. Ann. Ent. Soc. Am. 61, 722–729 (1968).CAS 
    Article 

    Google Scholar 
    81.Zchori-Fein, E. et al. A newly discovered bacterium associated with parthenogenesis and a change in host selection behawior in parasitoid wasps. PNAS 98, 12555–12560 (2001).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    82.Giorgini, M. et al. Rickettsia symbionts cause parthenogenic reproduction in the parasitoid wasp Pnigalio soemius (Hymenoptera: Eulophidae). Appl. Environ. 8, 2589–2599 (2010).Article 
    CAS 

    Google Scholar  More

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    Biobased and mechanically stiff lignosulfonate/cationic-polyelectrolyte/sugar complexes with coexisting ionic and covalent crosslinks

    1.Andrady AL. The plastic in microplastics: a review. Mar Pollut Bull. 2017;119:12–22.CAS 
    Article 

    Google Scholar 
    2.Akdogan Z, Guven B. Microplastics in the environment: a critical review of current understanding and identification of future research needs. Environ Pollut. 2019;254:113011.CAS 
    Article 

    Google Scholar 
    3.Dilkes-Hoffman LS, Pratt S, Lant PA, Laycock B. The role of biodegradable plastic in solving plastic solid waste accumulation. In: Al-Salem SM, editor. Plastics to energy. New York: William Andrew Publishing; 2019. p. 469–505.4.Reichert CL, Bugnicourt E, Coltelli MB, Cinelli P, Lazzeri A, Canesi I, et al. Bio-based packaging: materials, modifications, industrial applications and sustainability. Polymers. 2020;12:1558CAS 
    Article 

    Google Scholar 
    5.Reglero Ruiz JA, Trigo-López M, García FC, García JM. Functional aromatic polyamides. Polymers. 2017;9:414.Article 

    Google Scholar 
    6.Pilato L. Phenolic resins: a century of progress. New York: Springer; 2010.7.Ko HU, Zhai L, Park JH, Lee JY, Kim D, Kim J. Poly(vinyl alcohol)–lignin blended resin for cellulose-based composites. J Appl Polym Sci. 2018;135:46655.Article 

    Google Scholar 
    8.Shikinaka K, Nakamura M, Otsuka Y. Strong UV absorption by nanoparticulated lignin in polymer films with reinforcement of mechanical properties. Polymer. 2020;190:122254.CAS 
    Article 

    Google Scholar 
    9.Kargarzadeh H, Galeski A, Pawlak A. PBAT green composites: effects of kraft lignin particles on the morphological, thermal, crystalline, macro and micromechanical properties. Polymer. 2020;203:122748.CAS 
    Article 

    Google Scholar 
    10.Matsuoka T, Nonaka H. Wet extrusion of wood powder using a cellulose derivative. Jpn TAPPI J. 2020;74:516–24.Article 

    Google Scholar 
    11.Shen X, Berton P, Shamshina JL, Rogers RD. Preparation and comparison of bulk and membrane hydrogels based on Kraft-and ionic-liquid-isolated lignins. Green Chem. 2016;18:5607–20.CAS 
    Article 

    Google Scholar 
    12.Li H, Sun JT, Wang C, Liu S, Yuan D, Zhou X, et al. High modulus, strength, and toughness polyurethane elastomer based on unmodified lignin. ACS Sustain Chem Eng. 2017;5:7942–9.CAS 
    Article 

    Google Scholar 
    13.Dehne L, Vila C, Saake B, Schwarz KU. Esterification of Kraft lignin as a method to improve structural and mechanical properties of lignin-polyethylene blends. J Appl Polym Sci. 2017;134:44582.Article 

    Google Scholar 
    14.Dick TA, Couve J, Gimello O, Mas A, Robin JJ. Chemical modification and plasma-induced grafting of pyrolitic lignin. Evaluation of the reinforcing effect on lignin/poly (L-lactide) composites. Polymer. 2017;118:280–96.Article 

    Google Scholar 
    15.Ushimaru K, Morita T, Fukuoka T. Moldable and humidity-responsive self-healable complex from lignosulfonate and cationic polyelectrolyte. ACS Sustain Chem Eng. 2018;6:14831–7.CAS 
    Article 

    Google Scholar 
    16.Ushimaru K, Hamano Y, Morita T, Fukuoka T. Moldable material from ε-poly-l-lysine and lignosulfonate: mechanical and self-healing properties of a bio-based polyelectrolyte complex. ACS Omega. 2019;4:9756–62.CAS 
    Article 

    Google Scholar 
    17.Hellwig M, Henle T. Baking, ageing, diabetes: a short history of the Maillard reaction. Angew Chem Int Ed. 2014;53:10316–29.CAS 
    Article 

    Google Scholar 
    18.Henning C, Glomb MA. Pathways of the Maillard reaction under physiological conditions. Glycoconj J. 2016;33:499–512.CAS 
    Article 

    Google Scholar 
    19.Ushimaru K, Morita T, Fukuoka T. Bio-based, flexible, and tough material derived from ε-poly-l-lysine and fructose via the Maillard reaction. ACS Omega. 2020;5:22793–9.CAS 
    Article 

    Google Scholar 
    20.Ushimaru K, Morita T, Fukuoka T. A bio-based adhesive composed of polyelectrolyte complexes of lignosulfonate and cationic polyelectrolytes. J Wood Chem Technol. 2020;40:172–7.CAS 
    Article 

    Google Scholar 
    21.Zhang ZH, Zeng XA, Brennan CS, Ma H, Aadil RM. Preparation and characterisation of novelty food preservatives by Maillard reaction between ε-polylysine and reducing sugars. Int J Food Sci Technol. 2019;54:1824–35.CAS 
    Article 

    Google Scholar 
    22.Lay M, Thajudin NLN, Hamid ZAA, Rusli A, Abdullah MK, Shuib RK. Comparison of physical and mechanical properties of PLA, ABS and nylon 6 fabricated using fused deposition modeling and injection molding. Compos B Eng. 2019;176:107341.CAS 
    Article 

    Google Scholar 
    23.Bunn HF, Higgins PJ. Reaction of monosaccharides with proteins: possible evolutionary significance. Science. 1981;213:222–4.CAS 
    Article 

    Google Scholar 
    24.Suarez G, Rajaram RAMA, Oronsky AL, Gawinowicz MA. Nonenzymatic glycation of bovine serum albumin by fructose (fructation). Comparison with the Maillard reaction initiated by glucose. J Biol Chem. 1989;264:3674–9.CAS 
    Article 

    Google Scholar 
    25.Kim C, Yoshie N. Polymers healed autonomously and with the assistance of ubiquitous stimuli: how can we combine mechanical strength and a healing ability in polymers? Polym J. 2018;50:919–29.CAS 
    Article 

    Google Scholar 
    26.Gong JP, Katsuyama Y, Kurokawa T, Osada Y. Double-network hydrogels with extremely high mechanical strength. Adv Mater. 2003;15:1155–8.CAS 
    Article 

    Google Scholar 
    27.Gong JP. Why are double network hydrogels so tough? Soft Matter. 2010;6:2583–90.CAS 
    Article 

    Google Scholar 
    28.Ducrot E, Chen Y, Bulters M, Sijbesma RP, Creton C. Toughening elastomers with sacrificial bonds and watching them break. Science. 2014;344:186–9.CAS 
    Article 

    Google Scholar 
    29.Neal JA, Mozhdehi D, Guan Z. Enhancing mechanical performance of a covalent self-healing material by sacrificial noncovalent bonds. J Am Chem Soc. 2015;137:4846–50.CAS 
    Article 

    Google Scholar 
    30.Nakajima T. Generalization of the sacrificial bond principle for gel and elastomer toughening. Polym J. 2017;49:477–85.CAS 
    Article 

    Google Scholar 
    31.Yamini G, Shakeri A, Zohuriaan-Mehr MJ, Kabiri K. Cyclocarbonated lignosulfonate as a bio-resourced reactive reinforcing agent for epoxy biocomposite: from natural waste to value-added bio-additive. J CO2 Util. 2018;24:50–8.32.Szabó G, Romhányi V, Kun D, Renner K, Pukánszky B. Competitive interactions in aromatic polymer/lignosulfonate blends. ACS Sustain Chem Eng. 2017;5:410–9.Article 

    Google Scholar 
    33.Lee SI, Chun BC. Effect of EGMA content on the tensile and impact properties of poly (phenylene sulfide)/EGMA blends. Polymer. 1998;39:6441–7.CAS 
    Article 

    Google Scholar 
    34.Yang Y, Duan H, Zhang S, Niu P, Zhang G, Long S, et al. Morphology control of nanofillers in poly (phenylene sulfide): a novel method to realize the exfoliation of nanoclay by SiO2 via melt shear flow. Compos Sci Technol. 2013;75:28–34.CAS 
    Article 

    Google Scholar 
    35.Tao X, Nonaka H. Wet extrusion molding of wood powder with hydroxy-propylmethyl cellulose and with citric acid as a crosslinking agent. BioResources. 2021;16:2314–25.CAS 

    Google Scholar 
    36.Hasegawa D, Teramoto Y, Nishio Y. Molecular complex of lignosulfonic acid/poly (vinyl pyridine) via ionic interaction: characterization of chemical composition and application to material surface modifications. J Wood Sci. 2008;54:143–52.CAS 
    Article 

    Google Scholar 
    37.Wei C, Zhu X, Peng H, Chen J, Zhang F, Zhao Q. Facile preparation of lignin-based underwater adhesives with improved performances. ACS Sustain Chem Eng. 2019;7:4508–14.CAS 
    Article 

    Google Scholar  More

  • in

    Differential gene expression indicates modulated responses to chronic and intermittent hypoxia in corallivorous fireworms (Hermodice carunculata)

    1.Altieri, A. H. et al. Tropical dead zones and mass mortalities on coral reefs. Proc. Natl. Acad. Sci. 114, 3660–3665 (2017).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    2.Lehrter, J. C., Ko, D. S., Lowe, L. L. & Penta, B. Predicted effects of climate change on northern Gulf of Mexico hypoxia. In Modeling coastal hypoxia 173–214 (Springer, 2017).3.Breitburg, D. et al. Declining oxygen in the global ocean and coastal waters. Science 359, eaam7240 (2018).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    4.Nelson, H. R. & Altieri, A. H. Oxygen: The universal currency on coral reefs. Coral Reefs 38, 177–198 (2019).ADS 
    Article 

    Google Scholar 
    5.Hughes, D. J. et al. Coral reef survival under accelerating ocean deoxygenation. Nat. Clim. Change 10, 1–12 (2020).ADS 
    Article 

    Google Scholar 
    6.Murphy, J. W. & Richmond, R. H. Changes to coral health and metabolic activity under oxygen deprivation. PeerJ 4, e1956 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    7.Harborne, A. R., Rogers, A., Bozec, Y.-M. & Mumby, P. J. Multiple stressors and the functioning of coral reefs. Ann. Rev. Mar. Sci. 9, 5.1-5.24 (2017).Article 

    Google Scholar 
    8.Van Oppen, M. J. et al. Shifting paradigms in restoration of the world’s coral reefs. Glob. Change Biol. 23, 3437–3448 (2017).ADS 
    Article 

    Google Scholar 
    9.Montagna, P. A. & Ritter, C. Direct and indirect effects of hypoxia on benthos in Corpus Christi Bay, Texas, USA. J. Exp. Mar. Biol. Ecol. 330, 119–131 (2006).CAS 
    Article 

    Google Scholar 
    10.Pollock, M., Clarke, L. & Dubé, M. The effects of hypoxia on fishes: from ecological relevance to physiological effects. Environ. Rev. 15, 1–14 (2007).CAS 
    Article 

    Google Scholar 
    11.Seitz, R. D., Dauer, D. M., Llansó, R. J. & Long, W. C. Broad-scale effects of hypoxia on benthic community structure in Chesapeake Bay, USA. J. Exp. Mar. Biol. Ecol. 381, S4–S12 (2009).Article 

    Google Scholar 
    12.Diaz, R. J. & Rosenberg, R. Marine benthic hypoxia: A review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr. Mar. Biol. Ann. Rev. 33, 245–203 (1995).
    Google Scholar 
    13.Dean, T. L. & Richardson, J. Responses of seven species of native freshwater fish and a shrimp to low levels of dissolved oxygen. NZ J. Mar. Freshw. Res. 33, 99–106 (1999).Article 

    Google Scholar 
    14.Wannamaker, C. M. & Rice, J. A. Effects of hypoxia on movements and behavior of selected estuarine organisms from the southeastern United States. J. Exp. Mar. Biol. Ecol. 249, 145–163 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Richardson, J., Williams, E. K. & Hickey, C. W. Avoidance behaviour of freshwater fish and shrimp exposed to ammonia and low dissolved oxygen separately and in combination. NZ J. Mar. Freshwat. Res. 35, 625–633 (2001).Article 

    Google Scholar 
    16.McAllen, R., Davenport, J., Bredendieck, K. & Dunne, D. Seasonal structuring of a benthic community exposed to regular hypoxic events. J. Exp. Mar. Biol. Ecol. 368, 67–74 (2009).Article 

    Google Scholar 
    17.Ogino, T. & Toyohara, H. Identification of possible hypoxia sensor for behavioral responses in a marine annelid. Capitella teleta. Biol. Open 8, bio37630 (2019).
    Google Scholar 
    18.Lenihan, H. S. & Peterson, C. H. How habitat degradation through fishery disturbance enhances impacts of hypoxia on oyster reefs. Ecol. Appl. 8, 128–140 (1998).Article 

    Google Scholar 
    19.Li, F.-G., Chen, J., Jiang, X.-Y. & Zou, S.-M. Transcriptome analysis of blunt snout bream (Megalobrama amblycephala) reveals putative differential expression genes related to growth and hypoxia. PLoS ONE 10, e0142801 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    20.Sahlmann, A., Wolf, R., Holth, T. F., Titelman, J. & Hylland, K. Baseline and oxidative DNA damage in marine invertebrates. J. Toxicol. Environ. Health A 80, 807–819 (2017).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Zoccola, D. et al. Structural and functional analysis of coral Hypoxia Inducible Factor. PLoS ONE 12, e0186262 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    22.Díaz, R. J. & Rosenberg, R. Marine benthic hypoxia: A review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr. Mar. Biol. Annu. Rev. 33, 245–303 (1995).
    Google Scholar 
    23.Bodamer, B. L. & Bridgeman, T. B. Experimental dead zones: two designs for creating oxygen gradients in aquatic ecological studies. Limnol. Oceanogr. Methods 12, 441–454 (2014).CAS 
    Article 

    Google Scholar 
    24.Vaquer-Sunyer, R. & Duarte, C. M. Thresholds of hypoxia for marine biodiversity. Proc. Natl. Acad. Sci. 105, 15452–15457. https://doi.org/10.1073/pnas.0803833105 (2008).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    25.Branco, P. et al. Potamodromous fish movements under multiple stressors: Connectivity reduction and oxygen depletion. Sci. Total Environ. 572, 520–525 (2016).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    26.Hayes, D. S., Branco, P., Santos, J. M. & Ferreira, T. Oxygen depletion affects kinematics and shoaling cohesion of cyprinid fish. Water 11, 642 (2019).CAS 
    Article 

    Google Scholar 
    27.Grimes, C. J., Capps, C., Petersen, L. H. & Schulze, A. Oxygen consumption during and post hypoxia exposure in bearded fireworms (Annelida: Amphinomidae). J. Comp. Physiol. B 190, 681–689 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    28.Semenza, G. L. Hypoxia-inducible factor 1 (HIF-1) pathway. Sci. Stke 407, 1–3 (2007).29.Taylor, C. T. & McElwain, J. C. Ancient atmospheres and the evolution of oxygen sensing via the hypoxia-inducible factor in metazoans. Physiology 25, 272–279 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Wang, G. L., Jiang, B.-H., Rue, E. A. & Semenza, G. L. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. 92, 5510–5514 (1995).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.Kaelin, W. G. Jr. & Ratcliffe, P. J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 30, 393–402 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    32.Marques, I. J. et al. Transcriptome analysis of the response to chronic constant hypoxia in zebrafish hearts. J. Comp. Physiol. B. 178, 77–92 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    33.Schulze, A., Grimes, C. J. & Rudek, T. E. Tough, armed and omnivorous: Hermodice carunculata (Annelida: Amphinomidae) is prepared for ecological challenges. J. Mar. Biol. Assoc. UK. 97,1–6 (2017).34.Witman, J. D. Effects of predation by the fireworm Hermodice carunculata on milleporid hydrocorals. Bull. Mar. Sci. 42, 446–458 (1988).
    Google Scholar 
    35.Vreeland, H. & Lasker, H. Selective feeding of the polychaete Hermodice carunculata Pallas on Caribbean gorgonians. J. Exp. Mar. Biol. Ecol. 129, 265–277 (1989).Article 

    Google Scholar 
    36.Vargas-Ángel, B., Thomas, J. D. & Hoke, S. M. High-latitude Acropora cervicornis thickets off Fort Lauderdale, Florida, USA. Coral Reefs 22, 465–473 (2003).Article 

    Google Scholar 
    37.Miller, M., Marmet, C., Cameron, C. & Williams, D. Prevalence, consequences, and mitigation of fireworm predation on endangered staghorn coral. Mar. Ecol. Prog. Ser. 516, 187–194 (2014).ADS 
    Article 

    Google Scholar 
    38.Lucey, N. M., Collins, M. & Collin, R. Oxygen‐mediated plasticity confers hypoxia tolerance in a corallivorous polychaete. Ecol. Evol. 10, 1145–1157 (2019).39.Grimes, C. J., Paiva, P. C., Petersen, L. H. & Schulze, A. Rapid plastic responses to chronic hypoxia in the bearded fireworm, Hermodice carunculata (Annelida: Amphinomidae). Mar. Biol. https://doi.org/10.1007/s00227-020-03756-0 (2020).Article 

    Google Scholar 
    40.Yáñez-Rivera, B. & Salazar-Vallejo, S. I. Revision of Hermodice Kinberg, 1857 (Polychaeta: Amphinomidae). Sci. Mar. 75, 251–262 (2011).Article 

    Google Scholar 
    41.Ahrens, J. B. et al. The curious case of Hermodice carunculata (Annelida: Amphinomidae): Evidence for genetic homogeneity throughout the Atlantic Ocean and adjacent basins. Mol. Ecol. 22, 2280–2291 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Gorr, T. A., Cahn, J. D., Yamagata, H. & Bunn, H. F. Hypoxia-induced synthesis of hemoglobin in the crustacean Daphnia magna is hypoxia-inducible factor-dependent. J. Biol. Chem. 279, 36038–36047 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Li, T. & Brouwer, M. Hypoxia-inducible factor, gsHIF, of the grass shrimp Palaemonetes pugio: Molecular characterization and response to hypoxia. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 147, 11–19 (2007).Article 
    CAS 

    Google Scholar 
    44.Soñanez-Organis, J. G. et al. Molecular characterization of hypoxia inducible factor-1 (HIF-1) from the white shrimp Litopenaeus vannamei and tissue-specific expression under hypoxia. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 150, 395–405 (2009).
    Google Scholar 
    45.Wei, L. et al. Comparative studies of hemolymph physiology response and HIF-1 expression in different strains of Litopenaeus vannamei under acute hypoxia. Chemosphere 153, 198–204 (2016).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Giannetto, A. et al. Hypoxia-inducible factor α and Hif-prolyl hydroxylase characterization and gene expression in short-time air-exposed Mytilus galloprovincialis. Mar. Biotechnol. 17, 768–781 (2015).CAS 
    Article 

    Google Scholar 
    47.Philipp, E. E. et al. Gene expression and physiological changes of different populations of the long-lived bivalve Arctica islandica under low oxygen conditions. PLoS ONE 7, e44621 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    48.Sussarellu, R., Fabioux, C., Le Moullac, G., Fleury, E. & Moraga, D. Transcriptomic response of the Pacific oyster Crassostrea gigas to hypoxia. Mar. Genom. 3, 133–143 (2010).Article 

    Google Scholar 
    49.Woo, S. et al. Expressions of oxidative stress-related genes and antioxidant enzyme activities in Mytilus galloprovincialis (Bivalvia, Mollusca) exposed to hypoxia. Zool. Stud. 52, 15 (2013).ADS 
    Article 
    CAS 

    Google Scholar 
    50.Burgeot, T. et al. Oyster summer morality risks associated with environmental stress. Summer Mortality of Pacific Oyster Crassostrea Gigas. The Morest Project. Éd. Ifremer/Quæ, 107–151 (2008).51.David, E., Tanguy, A., Pichavant, K. & Moraga, D. Response of the Pacific oyster Crassostrea gigas to hypoxia exposure under experimental conditions. FEBS J. 272, 5635–5652 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    52.Hourdez, S. et al. Gas transfer system in Alvinella pompejana (Annelida polychaeta, Terebellida): Functional properties of intracellular and extracellular hemoglobins. Physiol. Biochem. Zool. 73, 365–373 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    53.Boutet, I., Jollivet, D., Shillito, B., Moraga, D. & Tanguy, A. Molecular identification of differentially regulated genes in the hydrothermal-vent species Bathymodiolus thermophilus and Paralvinella pandorae in response to temperature. BMC Genom. 10, 222 (2009).Article 
    CAS 

    Google Scholar 
    54.Eyre, B. D., Andersson, A. J. & Cyronak, T. Benthic coral reef calcium carbonate dissolution in an acidifying ocean. Nat. Clim. Change 4, 969–976 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    55.Huggett, J. & Griffiths, C. Some relationships between elevation, physico-chemical variables and biota of intertidal rock pools. Mar. Ecol. Prog. Ser. 29, 189–197 (1986).ADS 
    Article 

    Google Scholar 
    56.Kinsey, D. & Kinsey, E. Diurnal changes in oxygen content of the water over the coral reef platform at Heron I. Mar. Freshw. Res. 18, 23–34 (1967).Article 

    Google Scholar 
    57.Helly, J. J. & Levin, L. A. Global distribution of naturally occurring marine hypoxia on continental margins. Deep Sea Res. Part I 51, 1159–1168 (2004).CAS 
    Article 

    Google Scholar 
    58.Levin, L. A., Gage, J. D., Martin, C. & Lamont, P. A. Macrobenthic community structure within and beneath the oxygen minimum zone, NW Arabian Sea. Deep Sea Res. Part II 47, 189–226 (2000).ADS 
    Article 

    Google Scholar 
    59.Gallardo, V. et al. Macrobenthic zonation caused by the oxygen minimum zone on the shelf and slope off central Chile. Deep Sea Res. Part II 51, 2475–2490 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    60.Gooday, A. et al. Faunal responses to oxygen gradients on the Pakistan margin: a comparison of foraminiferans, macrofauna and megafauna. Deep Sea Res. Part II 56, 488–502 (2009).ADS 
    CAS 
    Article 

    Google Scholar 
    61.Prabhakar, N. R. & Semenza, G. L. Adaptive and maladaptive cardiorespiratory responses to continuous and intermittent hypoxia mediated by hypoxia-inducible factors 1 and 2. Physiol. Rev. 92, 967–1003 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    62.Du, S. N., Mahalingam, S., Borowiec, B. G. & Scott, G. R. Mitochondrial physiology and reactive oxygen species production are altered by hypoxia acclimation in killifish (Fundulus heteroclitus). J. Exp. Biol. 219, 1130–1138 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    63.Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    64.Bryant, D. M. et al. A tissue-mapped axolotl de novo transcriptome enables identification of limb regeneration factors. Cell Rep. 18, 762–776 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    65.Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494–1512 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    66.Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    67.Soneson, C., Love, M. I. & Robinson, M. D. Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences. F1000Research 4, 1–19 (2015).68.Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).CAS 
    Article 

    Google Scholar 
    69.Conesa, A., Nueda, M. J., Ferrer, A. & Talón, M. maSigPro: A method to identify significantly differential expression profiles in time-course microarray experiments. Bioinformatics 22, 1096–1102 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    70.Nueda, M.J., Tarazona, S., & Conesa, A. Next maSigPro: updating maSigPro bioconductor package for RNA-seq time series. Bioinformatics, 30, 2598–2602. https://doi.org/10.1093/bioinformatics/btu333 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    71.OmicsBox. Bioinformatics Made Easy, BioBam Bioinformatics. https://www.biobam.com/omicsbox (2019).72.Costa-Paiva, E. M., Schrago, C. G., Coates, C. J. & Halanych, K. M. Discovery of novel hemocyanin-like genes in Metazoans. Biol. Bull. 235, 134–151 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    73.Kanaoka, Y. & Urade, Y. Hematopoietic prostaglandin D synthase. Prostaglandins Leukot. Essent. Fatty Acids 69, 163–167 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    74.Altun, M. et al. Ubiquitin-specific protease 19 (USP19) regulates hypoxia-inducible factor 1α (HIF-1α) during hypoxia. J. Biol. Chem. 287, 1962–1969 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    75.Ogawa, M. et al. 17β-estradiol represses myogenic differentiation by increasing ubiquitin-specific peptidase 19 through estrogen receptor α. J. Biol. Chem. 286, 41455–41465 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    76.Isaacs, J. S. et al. Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1α-degradative pathway. J. Biol. Chem. 277, 29936–29944 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    77.Nallapalli, R. K. et al. Targeting filamin A reduces K-RAS–induced lung adenocarcinomas and endothelial response to tumor growth in mice. Mol. Cancer 11, 1–11 (2012).Article 
    CAS 

    Google Scholar 
    78.Feng, Y. et al. Filamin A (FLNA) is required for cell–cell contact in vascular development and cardiac morphogenesis. Proc. Natl. Acad. Sci. 103, 19836–19841 (2006).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    79.Muñoz-Chápuli, R. Evolution of angiogenesis. Int. J. Dev. Biol. 55, 345–351 (2011).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    80.Kim, S., Lee, M. & Choi, Y. K. The role of a neurovascular signaling pathway involving hypoxia-inducible factor and notch in the function of the central nervous system. Biomol. Ther. 28, 45 (2020).Article 

    Google Scholar 
    81.Nie, H., Wang, H., Jiang, K. & Yan, X. Transcriptome analysis reveals differential immune related genes expression in Ruditapes philippinarum under hypoxia stress: potential HIF and NF-κB crosstalk in immune responses in clam. BMC Genom. 21, 1–16 (2020).Article 
    CAS 

    Google Scholar  More

  • in

    A quantitative analysis of intensification in the ethnographic record

    1.Trigger, B. G. Sociocultural Evolution: Calculation and Contingency (Blackwell, 1998).2.Morgan, L. H. Ancient Society (Charles Kerr, 1877).3.Spencer, H. The Evolution of Society: Selections from Herbert Spencer’s Principles of Sociology (Univ. of Chicago Press, 1967).4.White, L. A. Energy and the evolution of culture. Am. Anthropol. 45, 335–356 (1943).Article 

    Google Scholar 
    5.Childe, V. G. The urban revolution. Town Plan. Rev. 21, 3–17 (1950).Article 

    Google Scholar 
    6.Adams, R. M. The Evolution of Urban Society: Early Mesopotamia and Prehispanic Mexico (Aldine, 1966).7.Wittfogel, K. A. Oriental Despotism: A Comparative Study of Total Power (Yale Univ. Press, 1957).8.Geertz, C. Agricultural Involution (Univ. of California Press, 1963).9.Boserup, E. The Conditions of Agricultural Growth: the Economics of Agrarian Change under Population Pressure (Aldine, 1965).10.Wolf, E. R. Peasants (Prentice-Hall, 1966).11.Binford, L. R. in New Perspectives in Archaeology (eds Binford, S. R. & Binford, L. R.) 421–449 (Aldine, 1968).12.Flannery, K. V. in The Domestication and Exploitation of Plants and Animals (eds Ucko, P. J. & Dimbleby, G. W.) 73–100 (Aldine, 1969).13.Sahlins, M. Stone Age Economics (Routledge, 2017).14.Cohen, M. N. The Food Crisis in Prehistory: Overpopulation and the Origins of Agriculture (Yale Univ. Press, 1977).15.Renfrew, C. in An Island Polity: the Archaeology of Exploitation in Melos (eds Renfrew, C. & Wagstaff, M.) 264–290 (Cambridge Univ. Press, 1982).16.Diamond, J. Guns, Germs, and Steel: the Fates of Human Societies (Norton, 1997).17.Johnson, A. W. & Earle, T. K. The Evolution of Human Societies: From Foraging Group to Agrarian State 2nd edn (Stanford Univ. Press, 2000).18.Trigger, B. G. Understanding Early Civilizations: a Comparative Study (Cambridge Univ. Press, 2003).19.Wenke, R. J. & Olszewski, D. I. Patterns in Prehistory: Humankind’s First Three Million Years 5th edn (Oxford Univ. Press, 2007).20.Scott, J. C. Against the Grain: a Deep History of the Earliest States (Yale Univ. Press, 2017).21.Hawkes, K., Kaplan, H., Hill, K. & Hurtado, A. M. Ache at the settlement: contrasts between farming and foraging. Hum. Ecol. 15, 133–161 (1987).Article 

    Google Scholar 
    22.Piperno, D. R. & Pearsall, D. M. The Origins of Agriculture in the Lowland Neotropics (Academic Press, 1998).23.Bronson, B. C. in Population Growth: Anthropological Implications (ed. Spooner, B.) 190–218 (MIT Press, 1972).24.Hunt, R. C. Labor productivity and agricultural development: Boserup revisited. Hum. Ecol. 28, 251–277 (2000).Article 

    Google Scholar 
    25.Bowles, S. Cultivation of cereals by the first farmers was not more productive than foraging. Proc. Natl Acad. Sci. USA 108, 4760–4765 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    26.Clark, C. & Haswell, M. The Economics of Subsistence Agriculture 4th edn (Macmillan, 1970).27.Netting, R. Smallholders, Householders: Farm Families and the Ecology of Intensive, Sustainable Agriculture (Stanford Univ. Press, 1993).28.Kirch, P. V. The Wet and the Dry: Irrigation and Agricultural Intensification in Polynesia (Univ. of Chicago Press, 1994).29.Stone, G. D. Settlement Ecology: the Social and Spatial Organization of Kofyar Agriculture (Univ. of Arizona Press, 1996).30.Logan, M. & Sanders, W. T. in The Valley of Mexico: Studies in Pre-Hispanic Ecology and Society (ed. Wolf, E.) 31–58 (Univ. of New Mexico Press, 1976).31.Sanders, W. T., Parsons, J. R. & Santley, R. S. The Basin of Mexico: the Evolution of a Civilization (Academic Press, 1979).32.Pimentel, D. & Pimentel, M. H. Food, Energy, and Society 3rd edn (CRC Press, 2007).33.Smil, V. Energy and Civilization: A History (MIT Press, 2017).34.Turgot, A. R. J. The Turgot Collection: Writings, Speeches, and Letters of Anne Robert Jacques Turgot, Baron de Laune (Ludwig von Mises Institute, 2011).35.Mill, J. S. The Collected Works of John Stuart Mill (Univ. of Toronto Press, 1963).36.Barkley, A. & Barkley, P. W. Principles of Agricultural Economics (Routledge, 2013).37.Naroll, R. A preliminary index of social development. Am. Anthropol. 58, 687–715 (1956).Article 

    Google Scholar 
    38.Carneiro, R. L. On the relationship between size of population and complexity of social organization. Southwest. J. Anthropol. 23, 234–243 (1967).Article 

    Google Scholar 
    39.Bettencourt, L. M., Samaniego, H. & Youn, H. Professional diversity and the productivity of cities. Sci. Rep. 4, 5393 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    40.Hanson, J. W., Ortman, S. G. & Lobo, J. Urbanism and the division of labour in the Roman Empire. J. R. Soc. Interface 14, 20170367 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Ortman, S. & Lobo, J. Smithian growth in a nonindustrial society. Sci. Adv. 6, eaba5694 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    42.Sandeford, D. S. Organizational complexity and demographic scale in primary states. R. Soc. Open Sci. 5, 171137 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    43.Adams, R. M. Heartland of Cities: Surveys of Ancient Settlement and Land Use on the Central Floodplain at the Euphrates (Univ. of Chicago Press, 1981).44.O’Brien, M., Mason, R. D., Lewarch, D. E. & Neely, J. A. Late Formative Irrigation Settlement below Monte Albán: Survey and Excavation on the Xoxocotlán Piedmont, Oaxaca, Mexico (Univ. of Texas Press, 1982).45.Billman, B. R. Irrigation and the origins of the southern Moche state on the north coast of Peru. Lat. Am. Antiq. 13, 371–400 (2002).Article 

    Google Scholar 
    46.Bandy, M. S. Energetic efficiency and political expediency in Titicaca Basin raised field agriculture. J. Anthropol. Archaeol. 24, 271–296 (2005).Article 

    Google Scholar 
    47.Liu, L. & Chen, X. The Archaeology of China: From the Late Paleolithic to the Early Bronze Age (Cambridge Univ. Press, 2012).48.Allen, R. C. Economic structure and agricultural productivity in Europe, 1300–1800. Eur. Rev. Econ. Hist. 4, 1–26 (2000).Article 

    Google Scholar 
    49.Hamilton, M. J., Walker, R. S., Buchanan, B. & Sandeford, D. S. Scaling human sociopolitical complexity. PLoS ONE 15, e0234615 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    50.Ortman, S. G., Lobo, J. & Smith, M. E. Cities: complexity, theory, and history. PLoS ONE 15, e0243621 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    51.Fujita, M., Krugman, P. & Mori, T. On the evolution of hierarchical urban systems. Eur. Econ. Rev. 43, 209–251 (1999).Article 

    Google Scholar 
    52.Bettencourt, L. M. The origins of scaling in cities. Science 340, 1438–1441 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    53.Samaniego, H. & Moses, M. E. Cities as organisms: allometric scaling of urban road networks. J. Transp. Land Use 1, 21–39 (2008).Article 

    Google Scholar 
    54.Smith, B. D. A cultural niche construction theory of initial domestication. Biol. Theory 6, 260–271 (2011).Article 

    Google Scholar 
    55.Winterhalder, B. & Smith, E. A. Analyzing adaptive strategies: human behavioral ecology at twenty-five. Evol. Anthropol. 9, 51–72 (2000).Article 

    Google Scholar 
    56.Kennett, D. J. & Winterhalder, B. (eds) Behavioral Ecology and the Transition to Agriculture (Univ. of California Press, 2006).57.Odling-Smee, J. F., Laland, K. N. & Feldman, M. W. Niche construction: the neglected process in evolution. Monographs in Population Biology No. 37 (Princeton Univ. Press, 2003).58.Mokyr, J. The Lever of Riches: Technological Creativity and Economic Progress (Oxford Univ. Press, 1992).59.Smith, B. D. General patterns of niche construction and the management of ‘wild’ plant and animal resources by small-scale pre-industrial societies. Phil. Trans. R. Soc. B 366, 836–848 (2011).PubMed 
    Article 

    Google Scholar 
    60.Turchin, P. in Cultural Evolution: Society, Technology, Language, and Religion (eds Richerson, P. J. & Christiansen, M. H.) 61–73 (MIT Press, 2013).61.Henrich, J. The Secret of Our Success: How Culture Is Driving Human Evolution, Domesticating Our Species, and Making Us Smarter (Princeton Univ. Press, 2016).62.Diamond, J. & Bellwood, P. Farmers and their languages: the first expansions. Science 300, 597–603 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    63.Bellwood, P. First Farmers: the Origins of Agricultural Societies (Blackwell, 2005).64.Murdock, G. P. et al. Ethnographic Atlas. World Cult. 10, 24–136 (1999).
    Google Scholar 
    65.Bocquet-Appel, J.-P. & Bar-Yosef, O. (eds) The Neolithic Demographic Transition and Its Consequences (Springer, 2008).66.Lesure, R. G., Martin, L. S., Bishop, K. J., Jackson, B. & Chykerda, C. M. The Neolithic demographic transition in Mesoamerica. Curr. Anthropol. 55, 654–664 (2014).Article 

    Google Scholar 
    67.Cohen, J. E. Population growth and Earth’s human carrying capacity. Science 269, 341–346 (1995).CAS 
    PubMed 
    Article 

    Google Scholar 
    68.DeLong, J. P. & Burger, O. Socio-economic instability and the scaling of energy use with population size. PLoS ONE 10, e0130547 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    69.Tuzin, D. Social Complexity in the Making: a Case Study among the Arapesh of New Guinea (Routledge, 2001).70.Boserup, E. Population and Technological Change: a Study of Long-Term Trends (Univ. of Chicago Press, 1981).71.Bettencourt, L. M., Lobo, J. & Strumsky, D. Invention in the city: increasing returns to patenting as a scaling function of metropolitan size. Res. Policy 36, 107–120 (2007).Article 

    Google Scholar 
    72.Rowley-Conwy, P. & Layton, R. Foraging and farming as niche construction: stable and unstable adaptations. Phil. Trans. R. Soc. B 366, 849–862 (2011).PubMed 
    Article 

    Google Scholar 
    73.Boivin, N. L. et al. Ecological consequences of human niche construction: examining long-term anthropogenic shaping of global species distributions. Proc. Natl Acad. Sci. USA 113, 6388–6396 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    74.Ullah, I. I., Chang, C. & Tourtellotte, P. Water, dust, and agro-pastoralism: modeling socio-ecological co-evolution of landscapes, farming, and human society in southeast Kazakhstan during the mid to late Holocene. J. Anthropol. Archaeol. 55, 101067 (2019).Article 

    Google Scholar 
    75.Turner, B. L. & Doolittle, W. E. The concept and measure of agricultural intensity. Prof. Geogr. 30, 297–301 (1978).Article 

    Google Scholar 
    76.Binford, L. R. Constructing Frames of Reference: an Analytical Method for Archaeological Theory Building Using Ethnographic and Environmental Data Sets (Univ. of California Press, 2001).77.Abrams, E. M. How the Maya Built Their World: Energetics and Ancient Architecture (Univ. of Texas Press, 1994).78.Erasmus, C. J. Monument building: some field experiments. Southwest. J. Anthropol. 21, 277–301 (1965).Article 

    Google Scholar 
    79.Durrenberger, E. P. Agricultural Production and Household Budgets in a Shan Peasant Village in Northwestern Thailand: a Quantitative Description (Ohio Univ. Center for International Studies, 1978).80.Grimes, W., Hodges, J., Nichols, R. & Tapp, J. A Study of Farm Organization in Central Kansas United States Department of Agriculture Bulletin No. 1296 (Government Printing Office, 1925).81.Barker, R., Herdt, R. & Rose, B. The Rice Economy of Asia (Resources for the Future, 1985).82.Cane, S. Australian aboriginal subsistence in the western desert. Hum. Ecol. 15, 391–434 (1987).Article 

    Google Scholar 
    83.Ortman, S. G., Cabaniss, A. H., Sturm, J. O. & Bettencourt, L. M. The pre-history of urban scaling. PLoS ONE 9, e87902 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    84.R Core Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, 2020).85.Geddes, W. R. The Land Dayaks of Sarawak Colonial Research Studies No. 14 (Her Majesty’s Stationary Office, 1954).86.Freeman, J. D. Iban Agriculture: a Report on the Shifting Cultivation of Hill Rice by the Iban of Sarawak Colonial Research Studies No. 18 (Her Majesty’s Stationary Office, 1955).87.Conklin, H. C. Hanunóo Agriculture: a Report on an Integral System of Shifting Cultivation in the Philippines (Food and Agricultural Organization of the United Nations, 1957).88.Moerman, M. Agricultural Change and Peasant Choice in a Thai Village (Univ. of California Press, 1968).89.Durrenberger, E. P. Rice production in a Lisu village. J. Southeast Asian Stud. 10, 139–145 (1979).Article 

    Google Scholar 
    90.Annual Report (International Rice Research Institute, 1966).91.Janlekha, K. A Study of the Economy of a Rice Growing Village in Central Thailand. PhD dissertation, Cornell Univ., 1955.92.Conelly, W. T. Agricultural intensification in a Philippine frontier community: impact on labor efficiency and farm diversity. Hum. Ecol. 20, 203–223 (1992).Article 

    Google Scholar 
    93.Chin, S. C. Agriculture and Subsistence in a Lowland Rainforest Kenyah Community. PhD dissertation, Yale Univ., 1984.94.Cramb, R. The use and productivity of labour in shifting cultivation: an East Malaysian case study. Agric. Syst. 29, 97–115 (1989).Article 

    Google Scholar 
    95.Hastorf, C. A. Agriculture and the Onset of Political Inequality before the Inka (Cambridge Univ. Press, 1993).96.Carter, W. E. New Lands and Old Traditions (Univ. of Florida Press, 1969).97.Truman, K. in Food and Farm: Current Debates and Policies Monographs in Economic Anthropology No. 7 (eds Gladwin, C. H. & Truman, K.) 161–178 (Univ. Press of America, 1989).98.Kirkby, A. Use of Land and Water Resources in the Past and Present Valley of Oaxaca, Mexico Memoirs of the University of Michigan Museum of Anthropology No. 5 (Museum of Anthropology, Univ. of Michigan, 1973).99.Lewis, O. Life in a Mexican Village: Tepoztlán Restudied (Univ. of Illinois Press, 1963).100.Tax, S. Penny Capitalism: a Guatemalan Indian Community (Univ. of Chicago Press, 1963).101.Cancian, F. Change and Uncertainty in a Peasant Economy: The Maya Corn Farmers of Zinacantan (Stanford Univ. Press, 1972).102.Stadelman, R. Maize Cultivation in Northwestern Guatemala Contributions to American Anthropology and History No. 33 (Carnegie Institution of Washington, 1940).103.Steggerda, M. Maya Indians of Yucatan (Carnegie Institution of Washington, 1941).104.Kelly, I. & Palerm, A. The Tajin Totonac: Part 1. History, Subsistence, Shelter and Technology Smithsonian Institution Institute of Social Anthropology No. 13 (United States Government Printing Office, 1952).105.Rappoport, R. Pigs for the Ancestors (Yale Univ. Press, 1968).106.Couture, M. D., Ricks, M. F. & Housley, L. Foraging behavior of a contemporary northern Great Basin population. J. Calif. Gt Basin Anthropol. 8, 150–160 (1986).
    Google Scholar 
    107.Noss, A. J. The economic importance of communal net hunting among the BaAka of the Central African Republic. Hum. Ecol. 25, 71–89 (1997).Article 

    Google Scholar 
    108.Hawkes, K., O’Connell, F. & Jones, N. B. Hadza children’s foraging: juvenile dependency, social arrangements, and mobility among hunter-gatherers. Curr. Anthropol. 36, 688–700 (1995).Article 

    Google Scholar 
    109.Lupo, K. D. & Schmitt, D. N. Small prey hunting technology and zooarchaeological measures of taxonomic diversity and abundance: ethnoarchaeological evidence from Central African forest foragers. J. Anthropol. Archaeol. 24, 335–353 (2005).Article 

    Google Scholar 
    110.Bliege Bird, R. & Bird, D. W. Why women hunt: risk and contemporary foraging in a Western Desert aboriginal community. Curr. Anthropol. 49, 655–693 (2008).Article 

    Google Scholar 
    111.O’Connell, J. F. & Hawkes, K. Food choice and foraging sites among the Alyawara. J. Anthropol. Res. 40, 504–535 (1984).Article 

    Google Scholar 
    112.Greaves, R. D. Ethnoarchaeological Investigation of Subsistence Mobility, Resource Targeting, and Technological Organization among Pume Foragers of Venezuela. PhD dissertation, Univ. of New Mexico, 1998.113.Eder, J. F. The caloric returns to food collecting: disruption and change among the Batak of the Philippine tropical forest. Hum. Ecol. 6, 55–69 (1978).Article 

    Google Scholar 
    114.O’Connell, J. F. & Hawkes, K. in Hunter-Gatherer Foraging Strategies: Ethnographic and Archaeological Analyses (eds Winterhalder, B. & Smith, E. A.) 99–125 (Univ. of Chicago Press, 1981).115.Jones, N. B., Hawkes, K. & Draper, P. Foraging returns of !Kung adults and children: why didn’t !Kung children forage? J. Anthropol. Res. 50, 217–248 (1994).Article 

    Google Scholar 
    116.Lee, R. B. in Man the Hunter (eds Lee, R. B. & DeVore, I.) 30–48 (Aldine, 1968).117.Hames, R. B. A comparison of the efficiencies of the shotgun and the bow in neotropical forest hunting. Hum. Ecol. 7, 219–252 (1979).Article 

    Google Scholar 
    118.Hawkes, K., Hill, K. & O’Connell, J. F. Why hunters gather: optimal foraging and the Ache of eastern Paraguay. Am. Ethnol. 9, 379–398 (1982).Article 

    Google Scholar 
    119.Ichikawa, M. An examination of the hunting-dependent life of the Mbuti. Afr. Study Monogr. 4, 55–76 (1983).
    Google Scholar 
    120.Terashima, H. Hunting life of the Bambote: an anthropological study of hunter-gatherers in a wooded savanna. Senri Ethnol. Stud. 6, 223–268 (1980).
    Google Scholar 
    121.Terashima, H. Mota and other hunting activities of the Mbuti archers: a socio-ecological study of subsistence technology. Afr. Study Monogr. 3, 71–85 (1983).
    Google Scholar 
    122.Arsdale, P. W. Activity patterns of Asmat hunter-gatherers: a time budget analysis. Aust. J. Anthropol. 11, 453–60 (1978).Article 

    Google Scholar 
    123.Baldwin, K. D. S. The Niger Agricultural Project, an Experiment in African Development (Blackwell, 1957).124.Stone, G. D., Netting, R. M. & Stone, M. P. Seasonality, labor scheduling, and agricultural intensification in the Nigerian savanna. Am. Anthropol. 92, 7–23 (1990).Article 

    Google Scholar 
    125.Panter-Brick, C. Motherhood and subsistence work: the Tamang of rural Nepal. Hum. Ecol. 17, 205–228 (1989).CAS 
    PubMed 
    Article 

    Google Scholar 
    126.Clark, G. A Farewell to Alms: A Brief Economic History of the World Vol. 25 (Princeton Univ. Press, 2008).127.Pospisil, L. J. Kapauku Papuan Economy (Dept of Anthropology, Yale Univ., 1963).128.Slicher Van Bath, B. H. The Agrarian History of Western Europe, AD 500–1850 (Edward Arnold, 1963).129.Goodell, G. Agricultural production in a traditional village of northern Khuzestan. Marbg. Geogr. Schriften 64, 243–289 (1975).
    Google Scholar 
    130.Cleave, J. H. African Farmers: Labor Use in the Development of Smallholder Agriculture (Praeger, 1974). More

  • in

    Potential local adaptation of corals at acidified and warmed Nikko Bay, Palau

    Seawater surface pH (total scale), Ωarag and temperatures (SST) showed a strong gradient at the entrance into the bay (Fig. 2a, b, e) and the seawater pH range (7.65–8.02) observed within the bay was equivalent to the ocean pH value from present to the value expected by the end of this century (IPCC 2013, RCP 8.5)29. The mean daytime seawater temperature within the bay was significantly warmer (31.8 ± 0.6 °C, mean ± S.D.) and had lower pH (7.83 ± 0.06), lower Ωarag, (2.44 ± 0.34) and higher pCO2 (619 ± 104 μatm) compared to parameters outside the bay (30.4 ± 0.1 °C, 8.02 ± 0.02, 391 ± 31 μatm, 3.63 ± 0.14, Wilcoxon-test, p  More

  • in

    Growth performance of five different strains of Nile tilapia (Oreochromis niloticus) introduced to Tanzania reared in fresh and brackish waters

    1.Fitzsimmons, K. M., Gonzalez-Alanis, P. & Martinez-Garcia, R. Why tilapia is becoming the most important food fish on the planet? In Proceedings of the 9th International Symposium on tilapia in Aquaculture, Shanghai Ocean University, Shanghai, China, 22-24 April 2011 8–16 (2011).2.FAO. The State of World Fisheries and Aquaculture. Meeting the sustainable development goals. Rome. Licence. CC BY-NC-SA 3.0 IGO (Food and Agriculture Organisation, 2018).3.ADB. An impact evaluation of the development of genetically improved farmed tilapia and their dissemination in selected countries. The Asian Development Bank, Manila, Philippines 90 (Asian Development Bank, 2004).4.Macaranas, J. M., Taniguchi, N., Pante, M. J. R., Capili, J. B. & Pullin, R. S. V. Electrophoretic evidence for extensive hybrid gene introgression into commercial Oreochromis niloticus (L.) stocks in the Philippines. Aquac. Res. 17, 249–258 (1986).CAS 
    Article 

    Google Scholar 
    5.ADB. An impact evaluation of the development of genetically improved farmed tilapia and their dissemination in selected countries. The Asian Development Bank, Manila, Philippines 137 (Asian Development Bank, 2005).6.Bradbeer, S. J. et al. Limited hybridization between introduced and critically endangered indigenous tilapia fishes in Northern Tanzania. University of Bristol. Hydrobiologia https://doi.org/10.1007/s10750-018-3572-5b (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    7.Shechonge, A. et al. Losing cichlid fish biodiversity: Genetic and morphological homogenization of tilapia following colonization by introduced species. Conserv. Genet. 19(5), 1199–1209 (2018).8.Gupta, M. V & Acosta, B. O. A review of global tilapia farming practices. Aquac. Asia 9, 7–12 (2004). 9.Eknath, A., Dey, M. M., Rye, M. & Gjerde, B. Selective breeding of Nile tilapia for Asia. In Proceedings of the 6th World Congress on Genetics Applied to Livestock Production, Armidale, Australia, University of New England. 27, 89–96 (1998).10.Ponzoni, R. W. et al. Genetic improvement of Nile tilapia (Oreochromis niloticus) with special reference to the work conducted by the WorldFish Center with the GIFT strain. Rev. Aquac. 3, 27–41 (2011).Article 

    Google Scholar 
    11.WorldFish. Genetically Improved Farmed Tilapia (GIFT). Key facts ongoing and future research. FactSheet. https://digitalarchive.worldfishcenter.org/bitstream/handle/20.500.12348/66/3880_2015-31.pdf?sequence=1&isAllowed=y (2015).
    12.Bolivar, R. Estimation of response to within-family selection for growth in Nile tilapia (Oreochromis niloticus). PhD. Dissertation, Dalhousie University, Halifax, N.S. Canada. 166 (1998).13.Tayamen, M. M. Nationwide dissemination of GET-EXCEL tilapia in the Philippines. In Proceeding of the Sixth International Symposium on Tilapia in Aquaculture. Bureau of Fisheries and Aquatic Resources, Manila, Philippines, and American Tilapia Association, Charles Town, West Virginia (ed. Bolivar, R,B., Mair, G.C and Fitzsimmons, K.) 74–85 (2004).14.Zimmerman, S. & Natividad, J. M. Comparative pond performance evaluation of GenoMar Supreme Tilapia GST 1 and GST 3 groups. In Proceeding of the Sixth International Symposium on Tilapia in Aquaculture. Bureau of Fisheries and Aquatic Resources, Manila, Philippines, and American Tilapia Association, Charles Town, West Virginia (ed. Bolivar, R.B., Mair, G.C and Fitzsimmons, K.) 89 (2004).
    15.Thodesen, J. et al. Genetic improvement of tilapias in China: Genetic parameters and selection responses in growth, survival and external color traits of red tilapia (Oreochromis spp.) after four generations of multi-trait selection. Aquaculture 416–417, 354–366 (2013).Article 

    Google Scholar 
    16.Ansah, Y. B., Frimpong, E. A. & Hallerman, E. M. Genetically-improved tilapia strains in Africa: Potential benefits and negative impacts. Sustain. 6, 3697–3721 (2014).Article 

    Google Scholar 
    17.Charo-karisa, H. Selection for growth of Nile tilapia (Oreochromis niloticus L.) in low-input environments. PhD Thesis, Wageningen University, The Netherlands (2006). 18.Kohinoor, A. H. M., Modak, P. C. & Hussain, M. G. Growth and production performance of red tilapia and Nile tilapia (Oreochromis niloticus L.) under low-input culture system. Bangladesh J. Fish Res. 3, 11–17 (1999).
    Google Scholar 
    19.Vadhel, N. et al. Red Tilapia: A candidate euryhaline species for aqua farming in Gujarat. J. Fish. 11(1), 048–050 (2017).
    Google Scholar 
    20.Felix, E., Avwemoya, F. E. & Abah, A. Some methods of monosex tilapia production: A review. Int. j. fish. aquat. res. 4(2), 42–49 (2019). 21.Fuentes-silva, C., Soto-zarazúa, G. M., Torres-pacheco, I. & Flores-rangel, A. Male tilapia production techniques: A mini-review. Afr. J. Biotechnol. 12, 5496–5502 (2013).
    Google Scholar 
    22.Wohlfarth, G. W. The unexploited potential of tilapia hybrids in aquaculture. Aquacult Fish Manage, 25, 781–788 (1994).23.Lahav, M. & Lahav, E. The development of all-male tilapia hybrids in Nir David. Bamidgeh. Isr. J. Aquac. 42, 58–61 (1990).
    Google Scholar 
    24.Siddiqui, A. Q. & Al-harbi, A. H. Evaluation of three species of tilapia, red tilapia and a hybrid tilapia as culture species in Saudi Arabia. Aquaculture 8486, 145–157 (1995).Article 

    Google Scholar 
    25.Gjerde, B. et al. Growth and survival in two complete diallele crosses with five stocks of Rohu carp (Labeo rohita). Aquaculture 209, 103–115 (2002).Article 

    Google Scholar 
    26.Mbiru, M. et al. Comparative performance of mixed-sex and hormonal sex-reversed Nile tilapia Oreochromis niloticus and hybrids (Oreochromis niloticus × Oreochromis urolepis hornorum) cultured in concrete tanks. Aquac. Int. 24, 557–566 (2015).Article 
    CAS 

    Google Scholar 
    27.Marengoni, N. G. et al. Morphological traits and growth performance of monosex male tilapia GIFT strain and Saint Peter®. Semin. Agrar. 36, 3399–3410 (2015).Article 

    Google Scholar 
    28.Eknath, A. E. & Acosta, B. O. Genetic improvement of farmed tilapias (GIFT) project: Final report, March to December 1997. International Center for Living Aquatic Resources Management (ICLARM), Makati City, Philippines 75 (1988). 29.Dan, N. C. & Little, D. C. The culture performance of monosex and mixed-sex new-season and overwintered fry in three strains of Nile tilapia (Oreochromis niloticus) in northern Vietnam. Aquaculture 184, 221–231. https://doi.org/10.1016/S0044-8486(99)00329-4 (2000).Article 

    Google Scholar 
    30.Kohinoor, A. H. M., Rahman, M. & Islam, S. Upgradation of genetically improved farmed tilapia (GIFT) strain by family selection in Bangladesh. Int. J. Fish. Aquat. Stud. 4, 650–654 (2016).
    Google Scholar 
    31.Ridha, M. Preliminary study on growth, feed conversion and production in non-improved and improved strains of the Nile tilapia Oreochromis niloticus. Fisheries and Marine Environment Department, Kuwait Institute for scientific Research, Salmiyah 22017, Kuwait (2016).32.Santos, B., Mareco, E. & Silva, M. Growth curves of Nile tilapia (Oreochromis niloticus) strains cultivated at different temperatures. Acta Sci. Anim. Sci. 35, 235–242 (2013).
    Google Scholar 
    33.Eknath, A. E. et al. Genetic improvement of farmed tilapias: Composition and genetic parameters of a synthetic base population of Oreochromis niloticus for selective breeding. Aquaculture 273, 1–14 (2007).CAS 
    Article 

    Google Scholar 
    34.Sukmanomon, S. et al. Genetic changes, intra- and inter-specific introgression in farmed Nile tilapia (Oreochromis niloticus) in Thailand. Aquaculture 324–325, 44–54 (2012).Article 

    Google Scholar 
    35.Anane-taabeah, G., Frimpong, E. A. & Hallerman, E. Aquaculture-mediated invasion of the Genetically Improved Farmed Tilapia (GIFT) into the Lower Volta Basin of Ghana. Diversity (Basel) 11, 188 (2019).CAS 
    Article 

    Google Scholar 
    36.Trinh, T. Q., Agyakwah, S. K., Khaw, H. L., Benzie, J. A. H. & Attipoe, F. K. Y. Performance evaluation of Nile tilapia (Oreochromis niloticus) improved strains in Ghana. Aquaculture 530, 735938 (2021).CAS 
    Article 

    Google Scholar 
    37.Canonico, G., Oceanic, N. & Arthington, A. H. The effects of introduced tilapias on native biodiversity. Aquat. Conserv. Mar. Freshw. Ecosyst. 15, 463–483 (2005).Article 

    Google Scholar 
    38.Lind, C. E., Brummett, R. E. & Ponzoni, R. W. Exploitation and conservation of fish genetic resources in Africa: Issues and priorities for aquaculture development and research. Rev. Aquac. 4, 125–141 (2012).Article 

    Google Scholar 
    39.URT. Ministry Livestock and Fisheries.Annual Report, Dodoma, Tanzania (United Republic of Tanzania, 2019).40.URT. Ministry of Livestock and Fisheries. Annual Report, Dodoma, Tanzania (United Republic of Tanzania, 2018).41.Mbiru, M. et al. Characterizing the genetic structure of introduced Nile tilapia (Oreochromis niloticus) strains in Tanzania using double digest RAD sequencing. Int. Aquac. https://doi.org/10.1007/s10499-019-00472-5 (2019).Article 

    Google Scholar 
    42.Kajungiro, R. A. et al. Population structure and genetic diversity of Nile Tilapia (Oreochromis niloticus) strains cultured in Tanzania. Front. Genet. 10, 1–12. https://doi.org/10.3389/fgene.2019.01269 (2019).Article 

    Google Scholar 
    43.Rothuis, A. et al. Aquaculture in East Africa: A regional approach. Wageningen, LEI Wageningen UR (University & Research Centre), LEI Report. IMARES C153/14| LEI. 14–120 (2014).44.URT. Vice President’s Office, Division of Environment: National Adaptation Programme of Action(NAPA, 2007).45.ATLAS. Climate change in Tanzania: Country risk profile. Task Order No. AID-OAA-I-14-00013 1–5 (Climate Change Adaptation, Thought Leadership and Assessments, 2018).46.Kassambara, A. ggpubr: ‘ggplot2’ Based Publication Ready Plot. 2019. https://rdrr.io/cran/ggpubr 2020/03/24 (2019).47.Shapiro, S. S. & Wilk, M. B. An analysis of variance test for normality (complete samples). Biometrika 52, 591–611 (1965).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    48.Evans, J. Straightforward Statistics for the Behavioral Sciences (Brooks/Cole Publishing, 1996).
    Google Scholar 
    49.Cohen, J. Statistical Power Analysis for the Behavioral Sciences 2nd edn. (Routledge, 1988).MATH 

    Google Scholar 
    50.Fox, J. & Weisberg, S. car: Companion to Applied Regression. Third Edition, Sage. Version 3.0–7 (2019). 51.Lenth, R., Singmann, H., Love, J., Buerkner, P. & Herve, M. emmeans: Estimated marginal means, aka least-squares means. R Package version 3.5.3. http://CRAN.R-project.org/package=emmeans, https://doi.org/10.1080/00031305.1980.10483031. (2020).52.Dey, M. M. et al. Performance and nature of genetically improved farmed tilapia: A bioeconomic analysis. Aquac. Econ. Manag. 4, 1–2 (2000).Article 

    Google Scholar 
    53.Sifa, L., Chenhong, L. & Dey, M. Cold tolerance of three strains of Nile tilapia, Oreochromis niloticus, in China. Aquaculture 213, 123–129 (2002).Article 

    Google Scholar 
    54.Cnaani, A., Gall, G. A. E. & Hulata, G. Cold tolerance of tilapia species and hybrids. Aquac. Int. 8, 289–298 (2000).Article 

    Google Scholar 
    55.Nandlal, S., Morris, C. W., Lagibalavu, M. & Ledua, E. A comparative evaluation of two tilapia strains in Fiji, 35–41. In Proceeding of the Fish Genetics Research in Member Countries and Institutions of the International Network on Genetics in Aquaculture. ICLARM Conf. Proc, 2-5 March 1999, Kuala Lumpur, Malaysia (eds. Gupta, M. V. & Acosta, B. O.) 64, (179), 35–42 (2001).56.Hussain, M. G. et al. Genetic evaluation of GIFT and existing strains of nile tilapia, Oreochromis niloticus L., under on-station and on-farm conditions in Bangladesh. Asian Fish. Sci. 13, 117–126 (2000).
    Google Scholar 
    57.Hopkins, K. Reporting fish growth: A review of the basics. J. World Aquac. Soc. 33, 173–179 (1992).Article 

    Google Scholar 
    58.Bhujel, R. C. On-farm feed management practices for Nile tilapia in Thailand. In On-Farm Feeding and Feed Management in Aquaculture. FAO Fisheries and Aquaculture Technical Paper No. 583. Rome. (ed. Hasan, M. R. & New, M. B.) 159–189 (2013).59.Volpato, G. & Fernandes, M. Social control of growth in fish. Braz. J. Med. Biol. Res. 27, 797–810 (1994).
    Google Scholar 
    60.Enquist, M. & Jakobsson, S. Decision making and assessment in the fighting behaviour of Nannacara anomala (Cichlidae, Pisces). Ethology 72, 143–153 (1986).Article 

    Google Scholar 
    61.Boscolo, C. N. P., Morais, R. N. & Freitas, E. G. Same-sized fish groups increase aggressive interaction of sex-reversed males Nile tilapia GIFT strain. Appl. Anim. Behav. Sci. 135, 154–159 (2011).Article 

    Google Scholar 
    62.Ebtehag Kamel, A. R. Evaluation of reproductive performance of tilapia strains and some of their crosses. J. Arab. Aquac. Soc. 6, 119–138 (2011).
    Google Scholar 
    63.Thoa, N. P., Ninh, N. H., Hoa, N. T., Knibb, W. & Diep, N. H. Additive genetic and heterotic effects in a 4 × 4 complete diallel cross-population of Nile tilapia (Oreochromis niloticus, Linnaeus, 1758) reared in different water temperature environments in different water temperature environments in Northern Viet. Aquac. Res. 47, 708–720 (2016).Article 
    CAS 

    Google Scholar 
    64.Ridha, M. T. Comparative study of growth performance of three strains of Nile tilapia, Oreochromis niloticus, L., at two stocking densities. Aquac. Res. 37, 172–179 (2006).Article 

    Google Scholar 
    65.Khan, S., Hossain, M. & Science, P. Production and economics of GIFT strain of tilapia (Oreochromis niloticus) in small seasonal ponds. Progress. Agric. 19(1), 97–104 (2008).Article 

    Google Scholar 
    66.Alam, M. B., Islam, M. A., Marine, S. S., Rashid, A. & Hossain, M. A. Growth performances of GIFT tilapia (Oreochromis niloticus) in Cage culture at the Old Brahmaputra river using different densities. J. SylhetAgril. Univ. 1(2), 265–271 (2014).
    Google Scholar 
    67.Matthew, M. T. et al. Growth performance evaluation of four wild strains and one current farmed strain of Nile tilapia in Uganda. Int. J. Fish. Aquat. Stud. 4, 594–598 (2016).
    Google Scholar 
    68.Shoko, A. P., Limbu, S. M., Mrosso, H. D. J., Mkenda, A. F. & Mgaya, Y. D. Effect of stocking density on growth, production and economic benefits of mixed sex Nile tilapia (Oreochromis niloticus) and African sharptooth catfish (Clarias gariepinus) in polyculture and monoculture. Aquac. Res. https://doi.org/10.1111/are.12463 (2014).Article 

    Google Scholar 
    69.Hasan, S. J., Mian, S., Rashid, A. H. & Rahmatullah, S. M. Effects of stocking density on growth and production of GIFT Tilapia (Oreochromis niloticus). Bangladesh. Fish. Res. 14, 45–53 (2010).
    Google Scholar 
    70.Rahman, M. M., Mondal, D. K., Amin, M. R. & Muktadir, M. G. Impact of stocking density on growth and production performance of monosex tilapia (Oreochromis niloticus) in ponds. Asian J. Med. Biol. Res. 2, 471–476 (2016).Article 

    Google Scholar 
    71.Li, S. et al. Improving growth performance and caudal fin stripe pattern in selected F6–F8 generations of GIFT Nile tilapia (Oreochromis niloticus L.) using mass selection. Aquac. Res. 37, 1165–1171 (2006).CAS 
    Article 

    Google Scholar 
    72.Dos Santos, B., Vander Silva, V. V., De, M. V., Mareco, E. A. & Salomão, R. A. S. Performance of Nile tilapia Oreochromis niloticus strains in Brazil: A comparison with Philippine strain. J. Appl. Anim. Res. 47, 72–78 (2019).Article 

    Google Scholar 
    73.Reis Neto, V. et al. Genetic parameters and trends of morphometric traits of GIFT tilapia under selection for weight gain. Sci. Agric. 71, 259–265 (2014).Article 

    Google Scholar 
    74.Gilbert, H. R. & Gregory, P. W. Some features of growth and development of Hereford cattle. J. Anim. Sci. 11, 3–16 (1952).Article 

    Google Scholar 
    75.Russell, W. S. T. The growth of Ayrshire cattle: An analysis of linear body measurements. J. Anim. Sci. 21, 217–226 (1975).Article 

    Google Scholar 
    76.Montoya-lópez, A., Moreno-arias, C., Tarazona-morales, A., Olivera-Angel, M. & Betancur, J. Body shape variation between farms of tilapia (Oreochromis sp.) in Colombian Andes using landmark based geometric morphometrics. Lat. Am. J. Aquat. Res. 47, 194–200 (2019).Article 

    Google Scholar 
    77.Bœuf, G. & Payan, P. How should salinity influence fish growth?. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 130(4), 411–423 (2001).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    78.Azevedo, R. V. et al. Responses of Nile tilapia to different levels of water salinity Rafael. Lat. Am. J. Aquat. Res. 43, 828–835 (2015).
    Google Scholar 
    79.Nguyen, H. N., Khaw, L. H., Ponzoni, R. W., Hamzah, A. & Kamaruzzaman, N. Can sexual dimorphism and body shape be altered in Nile tilapia (Oreochromis niloticus) by genetic means?. Aquaculture 272S1, S38–S46 (2007).Article 

    Google Scholar 
    80.Imre, I., McLaughlin, R. L. & Noakes, D. L. G. Phenotypic plasticity in brook charr: Changes in caudal fin induced by water flow. J. Fish Biol. 61, 1171–1181 (2002).Article 

    Google Scholar 
    81.Costa, C. et al. Genetic and environmental influences on shape variation in the European sea bass (Dicentrarchus labrax). Biol. J. Linn. Soc. 101, 427–436 (2010).Article 

    Google Scholar 
    82.Vehanen, T. & Huusko, A. Brown trout Salmo trutta express different morphometrics due to divergence in the rearing environment. J. Fish Biol. 79, 1167–1181 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    83.Ndiwa, T. C., Nyingi, D. W., Claude, J. & Agnèse, J.-F. Morphological variations of wild populations of Nile tilapia (Oreochromis niloticus) living in extreme environmental conditions in the Kenyan Rift-Valley. Environ. Biol. Fishes. https://doi.org/10.1007/s10641-016-0492-y (2016).Article 

    Google Scholar 
    84.Khaw, L. H., Ponzoni, R. W., Hamzah, A., Abu-bakar, K. R. & Bijma, P. Genotype by production environment interaction in the GIFT strain of Nile tilapia (Oreochromis niloticus). Aquaculture 326–329, 53–60 (2012).Article 

    Google Scholar 
    85.Kosai, P., Sathavorasmith, P., Jiraungkoorskul, K. & Jiraungkoorskul, W. Morphometric characters of Nile Tilapia
    (Oreochromis niloticus) in Thailand. Walailak Jour. Sci. and Tech. 11(10), 857–863 (2014). More

  • in

    Calcification in free-living coralline algae is strongly influenced by morphology: Implications for susceptibility to ocean acidification

    1.Foster, M. S. Rhodoliths between rocks and soft places. J. Phycol. 37, 659–667. https://doi.org/10.1046/j.1529-8817.2001.00195.x (2001).Article 

    Google Scholar 
    2.Riosmena-Rodríguez, R., Nelson, W. & Aguirre, J. Rhodolith/mäerl beds: A global perspective (Springer, 2017). https://doi.org/10.1007/978-3-319-29315-8.Book 

    Google Scholar 
    3.Nelson, W. A. Calcified macroalgae—critical to coastal ecosystems and vulnerable to change: a review. Mar. Freshw. Res. 60, 787–801. https://doi.org/10.1071/MF08335 (2009).CAS 
    Article 

    Google Scholar 
    4.Amado-Filho, G. M. et al. Rhodolith beds are major CaCO3 bio-factories in the tropical South West Atlantic. PLoS ONE 7, e35171. https://doi.org/10.1371/journal.pone.0035171 (2012).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    5.Smith, S. V. & Mackenzie, F. T. The role of CaCO3 reactions in the contemporary oceanic CO2 cycle. Aquat. Geochem. 22, 153–175. https://doi.org/10.1007/s10498-015-9282-y (2015).Article 

    Google Scholar 
    6.Amado-Filho, G.M., Bahia, R.G., Pereira-Filho, G.H. & Longo, L.L. South Atlantic rhodolith beds: Latitudinal distribution, species composition, structure and ecosystem functions, threats and conservation status. In Rhodolith/mäerl beds: A global perspective (eds, Riosmena-Rodríguez, R. et al.), Switzerland: Springer International Publishing; https://doi.org/10.1007/978-3-319-29315-8_12 (2017).7.Carvalho, V. F. et al. Environmental drivers of rhodolith beds and epiphytes community along the South Western Atlantic coast. Mar. Environ. Res. 154, 104827. https://doi.org/10.1016/j.marenvres.2019.104827 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    8.Legrand, E. et al. Species interactions can shift the response of a maerl bed community to ocean acidification and warming. Biogeosciences 14, 5359–5376. https://doi.org/10.5194/bg-14-5359-2017 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    9.Legrand, E. et al. Grazers increase the sensitivity of coralline algae to ocean acidification and warming. J. Sea Res. 148–149, 1–7. https://doi.org/10.1016/j.seares.2019.03.001 (2019).Article 

    Google Scholar 
    10.Legrand, E., Martin, S., Leroux, C. & Riera, P. Using stable isotope analysis to determine the effects of ocean acidification and warming on trophic interactions in a maerl bed community. Mar. Ecol. https://doi.org/10.1111/maec.12612 (2020).Article 

    Google Scholar 
    11.Burdett, H. L., Perna, G., McKay, L., Broomhead, G. & Kamenos, N. A. Community-level sensitivity of a calcifying ecosystem to acute in situ CO2 enrichment. Mar. Ecol. Prog. Ser. 587, 73–80. https://doi.org/10.3354/meps12421 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    12.Sordo, L., Santos, R., Barrote, I. & Silva, J. High CO2 decreases the long-term resilience of the free-living coralline algae Phymatolithon lusitanicum. Ecol. Evol. 8, 4781–4792. https://doi.org/10.1002/ece3.4020 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    13.Sordo, L., Santos, R., Barrote, I. & Silva, J. Temperature amplifies the effect of high CO2 on the photosynthesis, respiration, and calcification of the coralline algae Phymatolithon lusitanicum. Ecol. Evol. 9, 11000–11009. https://doi.org/10.1002/ece3.5560 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    14.Qui-Minet, Z. M. et al. Combined effects of global climate change and nutrient enrichment on the physiology of three temperate maerl species. Ecol. Evol. 9, 13787–13807. https://doi.org/10.1002/ece3.5802 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    15.Schubert, N. et al. Rhodolith primary and carbonate production in a changing ocean: the interplay of warming and nutrients. Sci. Total Environ. 676, 455–468. https://doi.org/10.1016/j.scitotenv.2019.04.280 (2019).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    16.Martin, S. & Hall-Spencer, J.M. Effects of ocean warming and acidification on rhodolith/mäerl beds. In Rhodolith/mäerl beds: A global perspective (eds. Riosmena-Rodríguez, R. et al.). Switzerland: Springer International Publishing; https://doi.org/10.1007/978-3-319-29315-8_3 (2017).17.Roleda, M. Y., Boyd, P. W. & Hurd, C. L. Before ocean acidification: calcifier chemistry lessons. J. Phycol. 48(4), 840–843. https://doi.org/10.1111/j.1529-8817.2012.01195.x (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    18.Dupont, S. & Pörtner, H. O. A snapshot of ocean acidification research. Mar. Biol. 160, 1765–1771. https://doi.org/10.1007/s00227-013-2282-9 (2013).CAS 
    Article 

    Google Scholar 
    19.Cyronak, T., Schulz, K. G. & Jokiel, P. L. The Omega myth: what really drives lower calcification rates in an acidifying ocean. ICES J. Mar. Sci. 73(3), 558–562. https://doi.org/10.1093/icesjms/fsv075 (2016).Article 

    Google Scholar 
    20.Falkenberg, L. J., Dupont, S. & Bellerby, R. G. Approaches to reconsider literature on physiological effects of environmental change: examples from ocean acidification research. Front. Mar. Sci. 5, 453. https://doi.org/10.3389/fmars.2018.00453 (2018).Article 

    Google Scholar 
    21.Cornwall, C. E., Comeau, S. & McCulloch, M. T. Coralline algae elevate pH at the site of calcification under ocean acidification. Global Change Biol. 23, 4245–4256. https://doi.org/10.1111/gcb.13673 (2017).ADS 
    Article 

    Google Scholar 
    22.Cornwall, C. E. et al. Resistance of corals and coralline algae to ocean acidification: physiological control of calcification under natural pH variability. Proc. Roy. Soc. B 285(1884), 20181168. https://doi.org/10.1098/rspb.2018.1168 (2018).CAS 
    Article 

    Google Scholar 
    23.Comeau, S., Cornwall, C. E., De Carlo, T. M., Krieger, E. & McCulloch, M. Similar controls on calcification under ocean acidification across unrelated coral reef taxa. Global Change Biol. 24, 4857–4868. https://doi.org/10.1111/gcb.14379 (2018).ADS 
    Article 

    Google Scholar 
    24.Comeau, S. et al. Flow-driven micro-scale pH variability affects the physiology of corals and coralline algae under ocean acidification. Sci. Rep. 9, 1–12. https://doi.org/10.1038/s41598-019-49044-w (2019).Article 

    Google Scholar 
    25.Comeau, S. et al. Resistance to ocean acidification in coral reef taxa is not gained by acclimatization. Nat. Clim. Chang. 9(6), 477–483. https://doi.org/10.1038/s41558-019-0486-9 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    26.Liu, Y. W., Sutton, J. N., Ries, J. B. & Eagle, R. A. Regulation of calcification site pH is a polyphyletic but not always governing response to ocean acidification. Sci. Adv. 6(5), aax1314. https://doi.org/10.1126/sciadv.aax1314 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    27.Donald, H. K., Ries, J. B., Stewart, J. A., Fowell, S. E. & Foster, G. L. Boron isotope sensitivity to seawater pH change in a species of Neogoniolithon coralline red alga. Geochim. Cosmochim. Acta 217, 240–253. https://doi.org/10.1016/j.gca.2017.08.021 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    28.Hofmann, L. C., Schoenrock, K. M. & de Beer, D. Arctic coralline algae elevate surface pH and carbonate in the dark. Front. Plant Sci. 9, 1416. https://doi.org/10.3389/fpls.2018.01416 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    29.Hurd, C. L. et al. Metabolically induced pH fluctuations by some coastal calcifiers exceed projected 22nd century ocean acidification: a mechanism for differential susceptibility. Global Change Biol. 17, 3254–3262. https://doi.org/10.1111/j.1365-2486.2011.02473.x (2011).ADS 
    Article 

    Google Scholar 
    30.Cornwall, C. E. et al. Diffusion boundary layers ameliorate the negative effects of ocean acidification on the temperate coralline macroalga Arthrocardia corymbosa. PLoS ONE 9, e97235. https://doi.org/10.1371/journal.pone.0097235 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    31.Hofmann, L. C., Koch, M. & de Beer, D. Biotic control of surface pH and evidence of light-induced H+ pumping and Ca2+-H+ exchange in a tropical crustose coralline alga. PLoS ONE 1, e0159057. https://doi.org/10.1371/journal.pone.0159057 (2016).CAS 
    Article 

    Google Scholar 
    32.McNicholl, C., Koch, M. S. & Hofmann, L. C. Photosynthesis and light-dependent proton pumps increase boundary layer pH in tropical macroalgae: A proposed mechanism to sustain calcification under ocean acidification. J. Exp. Mar. Biol. Ecol. 521, 151208. https://doi.org/10.1016/j.jembe.2019.151208 (2019).Article 

    Google Scholar 
    33.Hurd, C. L. & Pilditch, C. A. Flow-induced morphological variations affect diffusion boundary-layer thickness of Macrocystis pyrifera (Heterokontophyta, Laminariales). J. Phycol. 47, 341–351. https://doi.org/10.1111/j.1529-8817.2011.00958.x (2011).Article 
    PubMed 

    Google Scholar 
    34.Foster, M.S., Amado-Filho, G.M., Kamenos, N.A., Riosmena-Rodríguez, R. & Steller D.L. Rhodoliths and rhodolith beds. In Research and Discoveries: The Revolution of Science Through SCUBA (eds, Lang, M.A. et al.). Washington, D.C, USA: Smithsonian Institution Scholarly Press (2013).35.Melbourne, L. A., Denny, M. W., Harniman, R. L., Rayfield, E. J. & Schmidt, D. N. The importance of wave exposure on the structural integrity of rhodoliths. J. Exp. Mar. Biol. Ecol. 503, 109–119. https://doi.org/10.1016/j.jembe.2017.11.007 (2018).Article 

    Google Scholar 
    36.Farias, J. N., Riosmena-Rodríguez, R., Bouzon, Z., Oliveira, E. C. & Horta, P. A. Lithothamnion superpositum (Corallinales; Rhodophyta): First description for the Western Atlantic or rediscovery of a species?. Phycol. Res. 58, 210–216. https://doi.org/10.1111/j.1440-1835.2010.00581.x (2010).Article 

    Google Scholar 
    37.Vieira-Pinto, T. et al. Lithophyllum species from Brazilian coast: range extension of Lithophyllum margaritae and description of Lithophyllum atlanticum sp. nov. (Corallineales, Corallinophycidae, Rhodophyta). Phytotaxa 190, 355–369. https://doi.org/10.11646/phytotaxa.190.1.21 (2014).Article 

    Google Scholar 
    38.Sissini, M. N. et al. Mesophyllum erubescens (Corallinales, Rhodophyta)-so many species in one epithet. Phytotaxa 190, 299–319. https://doi.org/10.11646/phytotaxa.190.1.18 (2014).Article 

    Google Scholar 
    39.de Beer, D. & Larkum, A. Photosynthesis and calcification in the calcifying algae Halimeda discoidea studied with microsensors. Plant Cell Environ. 24, 1209–1217. https://doi.org/10.1046/j.1365-3040.2001.00772.x (2001).Article 

    Google Scholar 
    40.Hurd, C. L. Slow-flow habitats as refugia for coastal calcifiers from ocean acidification. J. Phycol. 51, 599–605. https://doi.org/10.1111/jpy.12307 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    41.Nash, M. C., Diaz-Pulido, G., Harvey, A. S. & Adey, W. Coralline algal calcification: A morphological and process-based understanding. PLoS ONE 14, e0221396. https://doi.org/10.1371/journal.pone.0221396 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    42.Burdett, H. L., Hennige, S. J., Francis, F. T. Y. & Kamenos, N. A. The photosynthetic characteristics of red coralline algae, determined using pulse amplitude modulation (PAM) fluorometry. Bot. Mar. 5, 499–509. https://doi.org/10.1515/bot-2012-0135 (2012).CAS 
    Article 

    Google Scholar 
    43.Noisette, F., Egilsdottir, H., Davoult, D. & Martin, S. Physiological responses of three temperate coralline algae from contrasting habitats to near-future ocean acidification. J. Exp. Mar. Biol. Ecol. 448, 179–187. https://doi.org/10.1016/j.jembe.2013.07.006 (2013).CAS 
    Article 

    Google Scholar 
    44.Martin, S., Cohu, S., Vignot, C., Zimmerman, G. & Gattuso, J. P. One-year experiment on the physiological response of the Mediterranean crustose coralline alga, Lithophyllum cabiochae, to elevated pCO2 and temperature. Ecol. Evol. 3(3), 676–693. https://doi.org/10.1002/ece3.475 (2013).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    45.Johnson, M. D., Moriarty, V. W. & Carpenter, R. C. Acclimatization of the crustose coralline alga Porolithon onkodes to variable pCO2. PLoS ONE 9(2), e87678. https://doi.org/10.1371/journal.pone.0087678 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    46.Cornwall, C. E. et al. A coralline alga gains tolerance to ocean acidification over multiple generations of exposure. Nat. Clim. Chang. 10, 143–146. https://doi.org/10.1038/s41558-019-0681-8 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    47.Cornwall, C. E. et al. Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proc. Roy. Soc. London Series B 280, 20132201. https://doi.org/10.1098/rspb.2013.2201 (2013).CAS 
    Article 

    Google Scholar 
    48.Boyd, P. W. et al. Biological responses to environmental heterogeneity under future ocean conditions. Global Change Biol. 22(8), 2633–2650. https://doi.org/10.1111/gcb.13287 (2016).ADS 
    Article 

    Google Scholar 
    49.Noisette, F. & Hurd, C. Abiotic and biotic interactions in the diffusive boundary layer of kelp blades create a potential refuge from ocean acidification. Funct. Ecol. 32(5), 1329–1342. https://doi.org/10.1111/1365-2435.13067 (2018).Article 

    Google Scholar 
    50.Johnson, M. D. et al. pH variability exacerbates effects of ocean acidification on a Caribbean crustose coralline alga. Front. Mar. Sci. 6, 150. https://doi.org/10.3389/fmars.2019.00150 (2019).Article 

    Google Scholar 
    51.Borowitzka, M. A. Photosynthesis and calcification in the articulated coralline red algae Amphiroa anceps and A foliacea. Mar. Biol. 62, 17–23. https://doi.org/10.1007/BF00396947 (1981).CAS 
    Article 

    Google Scholar 
    52.Chisholm, J. R. Calcification by crustose coralline algae on the northern Great Barrier Reef Australia. Limnol. Oceanogr. 45(7), 1476–1484. https://doi.org/10.4319/lo.2000.45.7.1476 (2000).ADS 
    CAS 
    Article 

    Google Scholar 
    53.Martin, S., Castets, M.-D. & Clavier, J. Primary production, respiration and calcification of the temperate free-living coralline alga Lithothamnion corallioides. Aquat. Bot. 85, 121–128. https://doi.org/10.1016/j.aquabot.2006.02.005 (2006).CAS 
    Article 

    Google Scholar 
    54.McNicholl, C. et al. Ocean acidification effects on calcification and dissolution in tropical reef macroalgae. Coral Reefs 39, 1635–1647. https://doi.org/10.1007/s00338-020-01991-x (2020).Article 

    Google Scholar 
    55.Kamenos, N. A. et al. Coralline algal structure is more sensitive to rate, rather than the magnitude, of ocean acidification. Global Change Biol. 19, 3621–3628. https://doi.org/10.1111/gcb.12351 (2013).ADS 
    Article 

    Google Scholar 
    56.Vogel, N. et al. Calcareous green alga Halimeda tolerates ocean acidification conditions at tropical carbon dioxide seeps. Limnol. Oceanogr. 60, 263–275. https://doi.org/10.1002/lno.10021 (2015).ADS 
    Article 

    Google Scholar 
    57.Vogel, N., Meyer, F. W., Wild, C. & Uthicke, S. Decreased light availability can amplify negative impacts of ocean acidification on calcifying coral reef organisms. Mar. Ecol. Prog. Ser. 521, 49–61. https://doi.org/10.3354/meps11088 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    58.McNicholl, C. & Koch, M. S. Irradiance, photosynthesis and elevated pCO2 effects on net calcification in tropical reef macroalgae. J. Exp. Mar. Biol. Ecol. 535, 151489. https://doi.org/10.1016/j.jembe.2020.151489 (2021).Article 

    Google Scholar 
    59.Schoenrock, K. M. et al. Influences of salinity on the physiology and distribution of the Arctic coralline algae, Lithothamnion glaciale (Corallinales, Rhodophyta). J. Phycol. 54, 690–702. https://doi.org/10.1111/jpy.12774 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    60.MAArE. Projeto de monitoramento ambiental da Reserva Biológica Marinha do Arvoredo e entorno. Florianópolis, Brazil: ICMBio/UFSC (2017).61.Kaandorp, J. A. & Kübler, J. E. The algorithmic beauty of seaweeds, sponges and corals (Springer, Heidelberg, 2001). https://doi.org/10.1007/978-3-662-04339-4.Book 
    MATH 

    Google Scholar 
    62.Leal, R. N., Bassi, D., Posenato, R. & Amado-Filho, G. M. Tomographic analysis for bioerosion signatures in shallow-water rhodoliths from the Abrolhos Bank Brazil. J. Coast. Res. 279, 306–309. https://doi.org/10.2112/11T-00006.1 (2012).Article 

    Google Scholar 
    63.Teichert, S. Hollow rhodoliths increase Svalbard’s shelf biodiversity. Sci. Rep. 4, 1–5. https://doi.org/10.1038/srep06972 (2014).CAS 
    Article 

    Google Scholar 
    64.Torrano-Silva, B. N., Ferreira, S. G. & Oliveira, M. C. Unveiling privacy: Advances in microtomography of coralline algae. Micron 72, 34–38. https://doi.org/10.1016/j.micron.2015.02.004 (2015).Article 
    PubMed 

    Google Scholar 
    65.Laforsch, C. et al. A precise and non-destructive method to calculate the surface area in living scleractinian corals using x-ray computed tomography and 3D modeling. Coral Reefs 27, 811–820. https://doi.org/10.1007/s00338-008-0405-4 (2008).ADS 
    Article 

    Google Scholar 
    66.Limaye, A. Drishti: a volume exploration and representation tool. In Developments in X-Ray Tomography VIII, San Diego, California, USA: SPIE Proc. 85060X; https://doi.org/10.1117/12.935640 (2012).67.Ahrens, J., Geveci, B. & Law, C. ParaView: An End-User Tool for Large Data Visualization. In Visualization Handbook (eds CD Hansen, CR Johnson) Oxford, UK: Elsevier; https://doi.org/10.1016/B978-012387582-2/50038-1 (2005).68.Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682. https://doi.org/10.1038/nmeth.2019 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    69.Rueden, C. T. et al. Image J2: ImageJ for the next generation of scientific image data. BMC Bioinformatics 18, 529. https://doi.org/10.1186/s12859-017-1934-z (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    70.Revsbech, N. P. An oxygen microsensor with a guard cathode. Limnol. Oceanogr. 34, 474–478. https://doi.org/10.4319/lo.1989.34.2.0474 (1989).ADS 
    CAS 
    Article 

    Google Scholar 
    71.de Beer, D. et al. A microsensor for carbonate ions suitable for microprofiling in freshwater and saline environments. Limnol. Oceanogr. Methods 6, 532–541. https://doi.org/10.4319/lom.2008.6.532 (2008).Article 

    Google Scholar 
    72.Jørgensen, B. B. & Revsbech, N. P. Diffusive boundary layers and the oxygen uptake of sediments and detritus 1. Limnol. Oceanogr. 30, 111–122. https://doi.org/10.4319/lo.1985.30.1.0111 (1985).ADS 
    Article 

    Google Scholar 
    73.Smith, S.V. & Kinsey, D.W. Calcification and organic carbon metabolism as indicated by carbon dioxide. In Coral Reefs: Research Methods. Monographs on Oceanographic Methodology (eds. Stoddart, D. & Johannes, R.). Paris: UNESCO (1978)74.Hansson, I. & Jagner, D. Evaluation of the accuracy of Gran plots by means of computer calculations: application to the potentiometric titration of the total alkalinity and carbonate content in sea water. Anal. Chim. Acta 75, 363–373. https://doi.org/10.1016/S0003-2670(01)82503-4 (1973).Article 

    Google Scholar 
    75.Bradshaw, A. L., Brewer, P. G., Sharer, D. K. & Williams, R. T. Measurements of total carbon dioxide and alkalinity by potentiometric titration in the GEOSECS program. Earth Planet. Sci. Lett. 55, 99–115. https://doi.org/10.1016/0012-821X(81)90090-X (1981).ADS 
    CAS 
    Article 

    Google Scholar 
    76.Stimson, J. & Kinzie, R. A. The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillophora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. J. Exp. Mar. Biol. Ecol. 153, 63–74. https://doi.org/10.1016/S0022-0981(05)80006-1 (1991).Article 

    Google Scholar 
    77.Naumann, M. S., Niggl, W., Laforsch, C., Glaser, C. & Wild, C. Coral surface area quantification-evaluation of established techniques by comparison with computer tomography. Coral Reefs 28, 109–117. https://doi.org/10.1007/s00338-008-0459-3 (2009).ADS 
    Article 

    Google Scholar 
    78.Veal, C. J., Holmes, G., Nunez, M., Hoegh-Guldberg, O. & Osborn, J. A comparative study of methods for surface area and three-dimensional shape measurements of coral skeletons. Limnol. Oceanogr. Methods 8, 241–253. https://doi.org/10.4319/lom.2010.8.241 (2010).Article 

    Google Scholar  More