Abstract
Lice of the family Echinophthiriidae are obligate and permanent ectoparasites of pinnipeds and sea otters. Morphological, ecological, and behavioral adaptations have enabled them to survive in their amphibian hosts. However, it has been shown experimentally that the eggs do not survive submerged. This physiological limitation restricts their reproductive events to the terrestrial periods of their hosts, mainly during molting and reproduction. We studied the reproductive strategies of Antarctophthirus lobodontis on crabeater seals (CS, n = 54) and A. carlinii on Weddell seals (WS, n = 54) from Danco Coast, Antarctic Peninsula, during the molting season. Lice were sexed and classified as adults or nymphs under a stereomicroscope. The 20.37% of the CS had potentially viable eggs and all the nymphal stages and adults. However, in the WS, we only found N3 and adults. Our results would suggest that A. lobodontis lays viable eggs that can survive immersion. Instead, the transmission of A. carlinii would be mainly by adults. According to previous studies, A. carlinii would reproduce during the reproductive season of WS. These reproductive strategies of seal lice would be related to the life history of their host, mainly to diving behavior and the haul-out patterns during their life cycle, reflecting the strong co-adaptation and co-evolution mechanisms between seals and lice. The differences in the population structure of the two species observed here may indicate that they are different species, or at least that they have undergone different co-evolutionary processes depending on the habit of their hosts.


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Abbreviations
- CS:
-
Crabeater seal
- WS:
-
Weddell seal
References
Adam PJ (2005) Lobodon carcinophaga. Mamm Species 772:1–14
Aznar FJ, Leonardi MS, Vera BB, Vales DG, Ameghino S, Raga JA, Crespo EA (2009) Population dynamics of Antarctophthirus microchir (Anoplura: Echinophthiriidae) in pups from South American sea lion, Otaria flavescens, in Northern Patagonia. Parasitology 136:293–303
Bengtson JL, Laake JL, Boveng PL, Cameron MF, Bradley Hanson M, Stewart BS (2011) Distribution, density, and abundance of pack-ice seals in the Amundsen and Ross Seas, Antarctica. Deep Sea Res Part II 58:1261–1276. https://doi.org/10.1016/j.dsr2.2010.10.037
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Machler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R Journal 9:378–400. https://doi.org/10.3929/ethz-b-000240890
Burns JM, Castellini MA, Testa JW (1999) Movements and diving behavior of weaned Weddell seal (Leptonychotes weddellii ) pups. Polar Biol 21:23–36. https://doi.org/10.1007/s003000050329
Burns JM, Costa DP, Fedak MA, Hindell MA, Bradshaw CJ, Gales NJ, McDonald B, Trumble SJ, Crocker DE (2004) Winter habitat use and foraging behavior of crabeater seals along the Western Antarctic Peninsula. Deep Sea Res Part II 51:2279–2303
Casaux R, Bertolin ML, Carlini A (2011) Feeding habits of three seal species at the Danco Coast, Antarctica: a re-assessment. Polar Biol 34:1615–1620. https://doi.org/10.1007/s00300-011-0994-1
Costa DP, Huckstadt LA, Crocker DE, McDonald BI, Goebel ME, Fedak MA (2010) Approaches to studying climatic change and its role on the habitat selection of Antarctic Pinnipeds. Integr Comp Biol 50:1018–1030. https://doi.org/10.1093/icb/icq054
Dong Y, Zhao M, Shao R (2022) Fragmented mitochondrial genomes of seal lice (family Echinophthiriidae) and gorilla louse (family Pthiridae): frequent minichromosomal splits and a host switch of lice between seals. BMC Genomics 23:283. https://doi.org/10.1186/s12864-022-08530-8
Erickson AW, Hanson MB (1990) Continental estimates and population trends of Antarctic ice seals. In: Kerry KR, Hempel G (eds) Antarctic Ecosystems. Springer, Heidelberg, pp 253–264
Gilbert JR, Erickson AW (1977) Distribution and abundance of seals in the pack ice of the Pacific sector of the Southern Ocean. Adaptations within Antarctic ecosystems. 703–740.
Hartig F, Lohse L (2021) DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models.
Hückstädt LA, Piñones A, Palacios DM, McDonald BI, Dinniman MS, Hofmann EE, Burns JM, Crocker DE, Costa DP (2020) Projected shifts in the foraging habitat of crabeater seals along the Antarctic Peninsula. Nat Clim Chang 10:472–477. https://doi.org/10.1038/s41558-020-0745-9
Kim K (1971) The sucking lice (Anoplura: Echinophthiriidae) of the northern fur seal; descriptions and morphological adaptation. Ann Entomol Soc Am 64:280–292. https://doi.org/10.1093/aesa/64.1.280
Kim (1975) Ecology and morphological adaptation of the sucking lice (Anoplura, Echinophthiriidae) on the northern fur seal. Rapport Et Procès Verbaux Des Réunions Du Conseil Permanent International Pour lExploration De La Mer 169:504–515
Kim KC (1972) Louse populations of the northern fur seal (Callorhinus ursinus).
Kooyman GL (1966) Maximum diving capacities of the Weddell seal, Leptonychotes weddelli. Science 151:1553–1554. https://doi.org/10.1126/science.151.3717.1553
Lenth R, Singmann H, Love J, Buerkner P, Herve M (2020) Emmeans: Estimated Marginal Means, Aka Least-Squares Means.
Leonardi MS, Lazzari CR (2014) Uncovering deep mysteries: the underwater life of an amphibious louse. J Insect Physiol 71:164–169. https://doi.org/10.1016/j.jinsphys.2014.10.016
Leonardi MS, Crespo EA, Raga JA, Aznar FJ (2013) Lousy mums: patterns of vertical transmission of an amphibious louse. Parasitol Res 112:3315–3323
Leonardi MS, Bobinac M, Negrete J (2016) Redescription of Antarctophthirus lobodontis (Anoplura: Echinophthiriidae) from the crabeater seal and identification key for Antarctic lice. Polar Biol 39:671–676. https://doi.org/10.1007/s00300-015-1822-9
Leonardi MS, Virrueta Herrera S, Sweet A, Negrete J, Johnson KP (2019) Phylogenomic analysis of seal lice reveals codivergence with their hosts. Syst Entomol 44:699–708. https://doi.org/10.1111/syen.12350
Leonardi MS, Crespo JE, Soto F, Lazzari CR (2021) How did seal lice turn into the only truly marine insects? Insects 13:46. https://doi.org/10.3390/insects13010046
Murray M (1976) Marine insects. North-Holland Publ, Co, Amsterdam
Murray MD, Nicholls DG (1965) Studies on the ectoparasites of seals and penguins. 1. The ecology of the louse Lepidophthirus macrorhini Enderlein on the southern elephant seal, Mirounga leonina (L). Aust J Zool 13:437–454
Murray M, Smith M, Soucek Z (1965) Studies on the ectoparasites of seals and penguins. 2. The ecology of the louse Antarctophthirus ogmorhini enderlein on the Weddell seal, Leptonychotes weddelli lesson. Aust J Zool 13:761–772
Nachtsheim DA, Jerosch K, Hagen W, Plötz J, Bornemann H (2017) Habitat modelling of crabeater seals (Lobodon carcinophaga) in the Weddell Sea using the multivariate approach Maxent. Polar Biol 40:961–976. https://doi.org/10.1007/s00300-016-2020-0
Nachtsheim DA, Ryan S, Schröder M, Jensen L, Oosthuizen WC, Bester MN, Hagen W, Bornemann H (2019) Foraging behaviour of Weddell seals (Leptonychotes weddellii) in connection to oceanographic conditions in the southern Weddell Sea. Prog Oceanogr 173:165–179. https://doi.org/10.1016/j.pocean.2019.02.013
Pinheiro J, Bates D, Debroy S, Sarkar D. (2021). Nlme: Linear and Nonlinear Mixed Effects Models.
R. Core Team (2020) R: a language and environment for statistical computing. R Found, Vienna
Siniff DB (1991) An overview of the ecology of Antarctic seals. Am Zool 31:143–149
Soto FA, Klaich MJ, Negrete J, Leonardi MS (2020) So happy together: juvenile crabeater seal behavior improves lice transmission. Parasitol Res 119:2059–2065. https://doi.org/10.1007/s00436-020-06704-5
Soto FA, Negrete J, Klaich MJ, Leonardi MS (2022) Effect of host age, sex and life stage on the prevalence and abundance of sucking lice on Weddell seal in the Antarctic Peninsula. An Acad Bras Ciênc 94:e20210566. https://doi.org/10.1590/0001-3765202220210566
Southwell C, Bengston J, Bester M, Blix AS, Bornemann H, Boveng P, Trathan P (2012) A review of data on abundance, trends in abundance, habitat use and diet of ice-breeding seals in the southern ocean. CCAMLR Sci 19:49–74
Stirling I (1969) Ecology of the Weddell seal in McMurdo Sound, Antarctica. Ecology 50:573–586. https://doi.org/10.2307/1936247
Wickham H (2016) Ggplot2: elegant graphics for data analysis. Springer Science+Business Media, New York
Acknowledgements
The study was financially and logistically supported by the Dirección Nacional del Antártico, Instituto Antártico Argentino. The permit for this work was granted by the Dirección Nacional del Antártico (Environmental Office). The authors support and defend the Argentinian Scientific Program, understanding science as an act of sovereignty.
Funding
This research was funded by the Agencia de Promoción Científica Tecnológica (PICT 2015–0082, PICT 2018–0537, PICT 2020–0400). This research was also funded by a Research Project from the Secretariat of Science and Technology of the UNPSJB (PI 1492- 80020180100018UP).
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FAS and MSL wrote the main manuscript text; FAS, MSL, JEC, and JN conceived the ideas and designed the methodology; FAS, MSL and JN, collected and processed the samples; FAS and JEC analyzed the samples and data; FAS, MSL, JEC, and JN led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
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Infestation parameters for each species; lice sex and classification as adults or nymphs
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Soto, F.A., Crespo, J.E., Negrete, J. et al. Tell me who you go with and I will tell you what you do: Antarctic seal lice behave differently. Mar Biol 171, 68 (2024). https://doi.org/10.1007/s00227-023-04386-y
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DOI: https://doi.org/10.1007/s00227-023-04386-y


