In May 2023, Frontiers adopted a new reporting platform to be Counter 5 compliant, in line with industry standards. The degree to which a species experiences fear or disgust is difficult to assess (Mendl et al., 2010), but regardless of the avoidance behavior, it is likely that many species have evolved with more than one enemy to contend with. In sum, this evolutionary framework stresses the importance of considering the impacts of multiple enemies with differential fitness costs and levels of risk. While these routes have their advantages, their viability remains moot. [9], The Lombok Strait is notable as one of the main passages for the Indonesian Throughflow (ITF) that exchanges water between the Indian Ocean and the Pacific Ocean. While the Indonesian archipelagic waters have been identified, how viable are these alternative waterways? For example, if a victim avoids conspecifics to reduce the likelihood of acquiring non-lethal enemies, this could simultaneously increase the likelihood of being detected and eaten by a lethal one. Anim. 75, 145150. How mammals stay healthy in nature: the evolution of behaviours to avoid parasites and pathogens. When imagining a pride of lions chasing down an antelope in sub-Saharan Africa, few would consider that these apex predators have any enemies of their own. In this section, we argue that the dichotomy of fitness effects between lethal and non-lethal enemies and the lifelong probability of a successful attack represent the two strongest selective pressures imposed by enemies on the evolution of resource allocation toward avoidance behaviors. 62, 839847. The fortnightly cycles of the oceans sea surface temperatures (SST) and Balis atmosphere have a peak seasonal cycle, which takes place during boreal summer. Given the geographical inconvenience of the passageways through the Indonesian archipelagic waters, it is reasonable to conclude that these routes through the Indonesian archipelago, though vital for international shipping, are more complementary than alternative routes to the primary maritime highway of the Straits of Malacca and Singapore. PSSA are management tools that can be used [1] We use satellite imagery and numerical modeling to investigate the characteristics ofLombok Strait nonlinear internal waves in relation to the dominant monsoon seasonality.Two basic wave types are identified, the first of which represents the wellknown arclikeinternal wave (AIW) that radiates uniformly away from its generation region near . It is recognized that parasites alone are important in sustaining diverse and complex food webs (Dunne et al., 2013). A PROJECTED increase of shipping traffic in the next decade has sparked concerns about traffic congestion in the Straits of Malacca and Singapore. Now recognized as a non-consumptive effect, the ecological and evolutionary impact of fear has been studied in a number of predator-prey systems within the last few decades. Aqua Satellite Dec 7, 2016 Oceanic Nonlinear Internal Solitary Waves From the Lombok Strait On November 1, 2016, NASA's Aqua satellite passed over Indonesia, allowing the Moderate Resolution Imaging Spectroradiometer (MODIS) on board to capture a stunning true-color image of oceanic nonlinear internal solitary waves from the Lombok Strait. R. Soc. Lombok Strait, a key channel connecting the Pacific and Indian Oceans, is one of the major passages for the Indonesian throughflow (ITF, Hautala et al., 1996, Hautala et al., 2001). Vessel LOMBOK STRAIT is a cargo ship sailing under the flag of Liberia. As a result, hosts have evolved to invest resources in behavioral or sensory traits that decrease the probability of infection. Oikos 127, 375380. Animals can thus navigate more safely through their environment, which has aptly been named the landscape of disgust (Weinstein et al., 2018a) as opposed to the landscape of fear in predator-prey systems (Laundr et al., 2001). (2018). The Makassar Strait stretches about 400 nautical miles from its northern gateway to its southern access. The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fevo.2020.564343/full#supplementary-material, Amoroso, C. R., Kappeler, P. M., Fichtel, C., and Nunn, C. L. (2019). [14] Improving defence forces at sea involves an emphasis in using the Indonesian navy to increase maritime security. (2018). Nevertheless the extremely deep channels of the Ombai-Wetar Straits provide an undetected access route for submarines between the Pacific Ocean and the Indian Ocean, making them collectively, an important waterway for American defence interests. Other alternatives such as the Lombok and Makassar Straits are much longer routes that would incur additional shipping costs estimated to be from around $84 to $220 billion per year, according to RSIS. [16] Alongside implementing Particularly Sensitive Sea Areas (PSSA) as a maritime strategy for the Lombok Strait, is the Traffic Separation Scheme (TSS) by the International Maritime Organisation (IMO), which is a traffic management route system. Lombok Strait, a key channel connecting the Pacific and Indian Oceans, is one of the major passages for the Indonesian throughflow (ITF, Hautala et al., 1996, Hautala et al., 2001). Proc. Cracked wood can also occur during the wintertime if a tree has this disease. As the Lombok Strait is situated between Bali and Lombok, it is an exit way for the Indonesian Throughflow (ITF) which connects the Pacific Ocean and the Indian Ocean. [16] Establishing the Lombok Strait as a Particularly Sensitive Sea Area (PSSA) contributes to the growth of the tuna fishing industry. Additionally, we predict that the evolution of resource allocation impacts the sensitivity of victims toward enemy cues. A trade-off between energy intake and exposure to parasites in oystercatchers feeding on a bivalve mollusc. It is therefore used by the largest ships of over 100,000 deadweight tonnage (DWT). This is because passage along this route consumes more time: a typical voyage from an Arabian Gulf port, Rastanurah, to Yokohama, Japan is about 6,600 nautical miles via the Malacca-Singapore route. The oceanography inside the Lombok Strait is highly complex, influenced by strong, north-south bi-directional tidal currents (up to 3.5 m/s), internal waves (observed wavelengths of ~2 -7.25 km . R. Soc. Each strategist incurs a negative fitness cost on the victims that they effectively consume or attack (see Figure 1 in Lafferty and Kuris, 2002), which varies in relation to the evolutionary history between both antagonistic species. Realistically, we could predict that this resource allocation translates into the amount of time that victims spend scanning their environment for enemy cues or how much they limit habitat use (see introduction). (2016). Alternative shipping routes through the Indonesian archipelagic waters have been identified, three in particular being the Sunda Strait, the Lombok and Makassar Straits and the Ombai-Weitar Straits near the island of Timor. These processes are now well established in predator-prey interactions (Gaynor et al., 2019), even though the overall impacts on prey population size are still poorly understood (Sheriff et al., 2020). doi: 10.1016/j.pt.2019.07.007, PubMed Abstract | CrossRef Full Text | Google Scholar, Buck, J. C., Weinstein, S. B., and Young, H. S. (2018). As for lethal enemies, this relationship is certainly positive, but it may not be linear. Proc. The route is used generally by local shipping including vessels proceeding between Australia and the Java Sea. (b) Geographical positions (II-3) to (II-6) define the axis line between Borneo (Kalimantan) and Celebes (Sulawesi) islands. Rev. This framework is then put into the more realistic context of a food web, which highlights the impact of trophic interactions and trophic level on the evolution of avoidance behaviors. Water exchange between the Pacific Ocean and the Indian Ocean takes place through the Lombok Strait. [14] These four choke points are used for national and international shipping routes. [14] As it is minimum 250 m (820 feet) deep much deeper than the Strait of Malacca ships that draw too much water to pass through the Malacca Strait (so-called "post Malaccamax" vessels) often use the Lombok Strait, instead. doi: 10.3377/004.047.0204, Bjork, K. E., Averbeck, G. A., and Stromberg, B. E. (2000). [8] Callidiopini species are identified to have been found on the islands of Bali and Lombok, which are divided by the Lombok Strait. From left to right, primary consumers in green include annelids, snails, and amphipods; secondary consumers in orange include schooling fishes and solitary fishes; tertiary consumers in red include birds and mammals. Behav. [7] The diverse range of mammals include rare and endangered whales and dolphins. A Mysterious Disease Afflicts Lobster Shells. Evol. The Lombok Strait is traversed by large vessels and has dense traffic. Fear of natural enemies in non-human animals is a concept dating back to the time of Darwin. Rips are one of the most dangerous things but aren't caused by waves. Ecology 94, 26972708. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Therefore, depending on the pressures imposed by the enemies they evolve with, victims may be more or less attuned to the environmental signals left by enemies. Evol. Adv. 90, 471477. Parasit. doi: 10.1098/rspb.1999.0835, Poulin, R. (2011). doi: 10.1016/B978-0-12-385897-9.00001-X, Poulin, R. (2014). doi: 10.1016/j.tree.2018.05.001, Costello, M. J. An enemy that successfully attacks a victim will either eliminate its fitness completely or reduce it partially. Parasite rates of discovery, global species richness and host specificity. [16] The growth of the tuna fishing industry in turn, contributes to the economy as it provides food security and income for residents along the coastline of Coral Triangle (CT) areas, and because the tuna breeding sites are foundational sources for tuna fishing companies who are producing tuna for consumers around the world. Parasitol. doi: 10.1093/icb/icw084, Curtis, V. A. (2008). Central assumptions of predator-prey models fail in a semi-natural experimental system. 44, 581589. Norris, K. (1999). Considering the above, it is sensible to combine the landscapes of fear and disgust into a broader landscape of enemies (Buck et al., 2018; Sarabian et al., 2018b), which we call here the landscape of peril. Only then could we understand how animals invest energy in their evolutionary toolkit of avoidance behaviors to safely navigate under the near constant threat of attack. 11, 533546. Carnivore carcasses are avoided by carnivores. However, comparatively little consideration has been given to the non-consumptive effects that parasites have on their hosts . For a primary consumer like the antelope, the non-consumptive effects of predation on their reproduction and even survival can sometimes surpass the direct effects of consumption (Sheriff and Thaler, 2014; MacLeod et al., 2018). Zool. Although trophically transmitted parasites are unlikely to have evolved to harm or kill their definitive hosts, since they help disperse the parasite into the environment, the host may have evolved traits to avoid heavily parasitized prey in order to mitigate the reward of eating conspicuous prey with the cost of acquiring heavy parasite burdens. Cognitive behaviour in Asian elephants: use and modification of branches for fly switching. A relatively narrow passageway where water flows from the Pacific Ocean into the Indian Ocean, the bottom is rough with both a shallow channel and a. Zoo Wildl. Evolution of pathogen and parasite avoidance behaviours. Are There Any Differences Between An Ocean Channel And A Strait. 35, 835847. In fact, it is likely that every metazoan species has evolved with at least one parasite (Poulin, 2014; Costello, 2016), therefore it is reasonable to assume that no animal species is devoid of natural enemies (now referred to simply as enemies). Yearly, about 2, 280 ships transit the Sunda Strait carrying in total some 100 million tonnes of cargo valued at US$5 billion. (2010) revealed that ITF had . 11:e1001579. [14] Issues particularly affecting the Lombok Strait include: piracy, illegal fishing, human trafficking, smuggling of goods, armed robberies and terrorism. [7] The statistics of fisheries activities along Indonesian waters was that an annual catch of more than 4.5 million tonnes occurred in 2006 and the catches between 1996-1997 included 1424 manta rays, 18 whale sharks, 312 other shark species, 4 minke whales, 326 dolphins, 577 pilot whales, 789 marlin, 84 turtles, and 9 dugongs. Even though the Lombok-Makassar route is much safer as it is relatively wide and deep and does not pose significant navigational hazards, it is not as navigationally convenient as the Straits of Malacca and Singapore. doi: 10.1016/s0169-5347(02)02615-0, Lafferty, K. D., and Kuris, A. M. (2009). Since animals likely evolve in the presence of multiple natural enemies, they must adopt a range of avoidance behaviors to navigate through the resulting landscape of peril. Therefore, in line with recent efforts to combine the landscapes of fear and disgust, we offer a theoretical framework to better understand the impacts of natural enemies on the evolution of trait-mediated avoidance behaviors in animals. Int. The Lombok Strait is 60 km long. Climate change occurs as the Indonesian Throughflow (ITF) contributes to the contained heat content in the strait and its sea surface temperatures (SST). Stop . Received: 21 May 2020; Accepted: 02 September 2020;Published: 18 September 2020. Lethal natural enemies do not necessarily kill their victims, but effectively eliminate victim fitness. Note that, for mammals, only one species was available from the dataset. Science 359, 12131214. 373:20170195. doi: 10.1098/rstb.2017.0195, Sarabian, C., Curtis, V., and McMullan, R. (2018b). These predictions are then verified with recent examples in the literature, putting into evolutionary context the landscape of peril. Unlike the Straits of Malacca and Singapore which is about 1.3 nautical miles at its narrowest point at the Philips Channel, the Sunda Strait is much broader; about 13 nautical miles wide at its narrowest. Parasites affect food web structure primarily through increased diversity and complexity. Book: Tetebatu Rice Terraces Private Tour (includes waterfall and Monkey Forest) 5. This high sensitivity results in the aphid losing a considerable amount of time away from the leaf, resulting in a reduction of energy intake. [3], Biologists believe it was the depth of the Lombok Strait itself that kept the animals on either side isolated from one another. Patterns of predation in a diverse predator-prey system. The arc-like internal wave and the irregular internal wave are wave patterns which occur as a result of seasonal influences. Sci. Here, you'll also catch a great view of Rinjani but there are also plenty of opportunities for waterfall chasing. The Lombok Strait is notable as one of the main passages for the Indonesian Throughflow (ITF) that exchanges water between the Indian Ocean and the Pacific Ocean. As enemies go, predators and parasites are but broad generalizations of a multitude of trophic strategies that exist, each one having its own fitness cost on the victims that are successfully attacked (Lafferty and Kuris, 2002). [7] The Lombok Strait is abundantly inhabited by the longnosed spinner dolphin (S. longirostris) and is commonly inhabited by the pantropical spotted dolphin (S. attenuata), bottlenose dolphin (T. truncatus), and the Southeast Asian spinner dolphin (Stenella longirostris roseiventris). doi: 10.1371/journal.pbio.1001579, Fill, A., Long, E. Y., and Finke, D. L. (2012). Sitka black-tailed deer (Odocoileus hemionus sitkensis) adjust habitat selection and activity rhythm to the absence of predators. He contributed this article especially to RSIS Commentaries. [1] Biol. Five distinct hydrocarbonoclastic marine bacterial species and two species from the Bacillus genera family, are bacterial strains that have been identified in the Lombok Strait. As a result, compared to the Straits of Malacca and Singapore route, both the Sunda and Lombok-Makassar passageways are little used by international traffic. Visit The Gili Islands. Two basic wave types are identified, the first of which represents the well-known arc-like internal wave (AIW) that radiates uniformly away from its generation region near the sill in regular sequences of ranked solitons. R. Soc. Trophic strategies in animals are not limited to predators and parasites. This affected area will often look and feel wetter than surrounding wood and could ooze slime. These straits are part of Indonesias archipelagic waters and have been designated by Indonesia as archipelagic sea lanes. Oikos 118, 801806. This depends ultimately on the selective pressures or risk imposed by enemies, which can be measured with abundance, lethality, or species richness (Bordes and Morand, 2009). These parasites can increase the likelihood that the intermediate host gets eaten by the definitive host through alteration of its behavior or appearance, making it more conspicuous (see Moore, 2002 for examples). doi: 10.1371/journal.pone.0116569, Lafferty, K. D., Allesina, S., Arim, M., Briggs, C. J., de Leo, G., Dobson, A. P., et al. It connects the Indian Ocean to the Java Sea. [4] They shared the Asian fauna. The Ombai Strait is located between the islands of Alor and Timor, and its counterpart, the Wetar Strait, is located between the northern coast of Timor and the southern coast of Wetar. doi: 10.1890/13-0396.1, Mendl, M., Burman, O. H. P., and Paul, E. S. (2010). Evol. Mitey costly: energetic costs of parasite avoidance and infection. The UN Secretary General has identified seven threats to maritime security in the Report on Oceans and the Law of the Sea 2008, which are: terrorist acts against shipping, offshore installations and other maritime interests, illicit trafficking in weapons of mass destruction, illicit trafficking in drugs, human trafficking, IUU fishing, and unlawful damage to the marine environment. doi: 10.1126/science.aas8694, Weinstein, S. B., Moura, C. W., Mendez, J. F., and Lafferty, K. D. (2018b). Behav. doi: 10.1016/j.ijpara.2014.02.003, Raffel, T. R., Martin, L. B., and Rohr, J. R. (2008). For example, oystercatchers consume mainly medium-sized cockles and avoid larger, energy-rich cockles that are likelier to have heavy parasite loads (Norris, 1999). Med. 89, 13021316. [13] The flow of the strait waters also makes it distinctive as it consists of a layered structure: the upper layer has a permanent southward flow and the lower layer has a reversing southward-northward flow. 266, 17031709. Therefore, a primary consumer like an amphipod may invest heavily into avoiding lethal enemies, whereas a secondary consumer like a solitary fish may invest relatively more resources toward non-lethal ones. Biol. 277, 28952904. [18] This is because the Strait of Malacca has become narrow and shallower, and shipping traffic has become busy each year, which would increase the risk of vessel collisions. [18] With businesses supporting this shift, this would result in Indonesia becoming one of the worlds biggest bunkering ports alongside Singapore. They are found to be of various colours: yellow, opaque, white, and purple. Growing shipping traffic congestion in the Straits of Malacca and Singapore has led to a search for alternative shipping routes. doi: 10.1111/1365-2656.13213, Sheriff, M. J., and Thaler, J. S. (2014). Behav. The ocean heat content of the Lombok Strait is determined by ocean-atmosphere interactions. 74, 140. The Lombok Strait (Indonesian: Selat Lombok), is a strait of the Bali Sea connecting to the Indian Ocean, and is located between the islands of Bali and Lombok in Indonesia. Anim. Afr. Wolves, elk, and bison: reestablishing the landscape of fear in Yellowstone National Park, USA. Here, the trade-off between nutrition and parasitism appears to depend mainly on the infection status of the sheep. 'Get used to it', experts warn", "The Importance of Establishing Particularly Sensitive Sea Areas in Lombok Strait: Maritime Security Perspective", https://sydney.primo.exlibrisgroup.com/discovery/fulldisplay?&context=PC&vid=61USYD_INST:sydney&docid=cdi_doaj_primary_oai_doaj_org_article_236d86b359084ba1889ee2b5b16c26b1, "Lombok, Makassar Straits Could Replace Malacca Strait as Main Sea Trading Lane, Says Indonesian Government", https://en.wikipedia.org/w/index.php?title=Lombok_Strait&oldid=1158003616, This page was last edited on 1 June 2023, at 10:33. R. Soc. As the Malacca Strait would no longer be able to cope with shipping traffic by the next 1020 years, the Indonesian Government encourages voyages to pass through the Lombok Strait instead. Oecologia 176, 607611. Such activities could result in the loss of foraging opportunities and potential energy intake. This is because majority of the worlds crude oil are traded along the route of the Lombok Strait. Hosts can avoid getting infected through changes in behavior (Hart and Hart, 2018), such as limiting interactions with conspecifics that appear infected (Stephenson et al., 2018), directly avoiding parasitic infective stages through the detection of cues (Strauss et al., 2019), or changing feeding habits (Sarabian et al., 2018a) or habitat use (Amoroso et al., 2019). If a certain victim evolves with a particular set of enemies due mainly to its position in the food web, it is possible that others lessen this particular pressure by growing larger. Ecol. (C) How victim populations theoretically evolve to allocate energy toward avoidance behaviors under the risk imposed by natural enemies. doi: 10.1638/1042-7260(2000)031[0056:papsof]2.0.co;2, Bonnot, N. C., Morellet, N., Hewison, A. J. M., Martin, J.-L., Benhamou, S., and Chamaille-Jammes, S. (2016). Animals at the base or at the top of the food web probably evolve with different ratios of lethal to non-lethal enemies. A plan to build a bridge across the Sunda Strait to connect Java and Sumatra is under study. [5], The Lombok Strait is abundant of flora and fauna species which have been well explored through Balis diving tourism. But in the early hours of April 21, the 44 year-old KRI Nanggala 402 submarine dropped out of contact and plummeted 838 metres to the ocean floor, taking 53 crew members with it. Thus, they shared Asian fauna. What About Trophically Transmitted Parasites? From these data, we are able to observe that the total number of lethal enemies, along with the ratio of lethal to non-lethal enemies, decrease in victims as we move up the food web of aquatic and semi-aquatic animal groups (Figure 2 and Supplementary Material). Sheep avoidance of faeces-contaminated patches leads to a trade-off between intake rate of forage and parasitism in subsequent foraging decisions. Ecol. Integr. So, if larger animals harbor more diverse parasite communities than do smaller ones in general, it is reasonable to assume that they evolved to invest relatively more in their avoidance behaviors against non-lethal enemies. These commentaries may be reproduced with prior permission from RSIS and due credit to the author(s) and RSIS. Another possible selective pressure imposed by enemies is the loss of energy intake or foraging opportunities due to the time victims spend detecting enemy cues or avoiding patches of food. (2013). However, the composition of enemy types for a particular victim could depend on its relative position in the food web, in addition to other characteristics such as body size or sociality. doi: 10.1006/anbe.1994.1209, Hart, B. L., and Hart, L. A. PLoS Biol. A., and Werner, E. E. (2013). Ecol. The numbers for each animal group are median values calculated for a number of species that were included in each group (Supplementary Material). Physiol. [12] The tide flow is controlled through Nusa Penida Sill (NPS), reaching 350 m in depth. Therefore, we argue that a loss of foraging opportunities is highly variable and context-dependent and represents a weaker selective pressure. Ecology 92, 2007. doi: 10.1890/11-0374.1, Keywords: avoidance behavior, fear, disgust, natural enemy, predator, parasite, non-consumptive effect, Citation: Doherty J-F and Ruehle B (2020) An Integrated Landscape of Fear and Disgust: The Evolution of Avoidance Behaviors Amidst a Myriad of Natural Enemies. If a victim evolves with lethal and non-lethal enemies that impose similar levels of risk, we predict that more energy would be invested into avoiding the lethal enemy, simply because of the potential fitness loss it imposes. Oceanic tidal mixing occurs in shallow seas and near-coastal areas. Therefore, even if non-lethal enemies pose less risk than lethal ones, we would still expect victims to invest resources into avoidance behaviors proportionally to the risk imposed by non-lethal enemies (e.g., lions avoiding carcasses, see introduction). Parasitic castration: the evolution and ecology of body snatchers. Sci. B Biol. The Lombok Strait has a maximum depth of 250 m or 820 feet. To date, there are only a few studies that simultaneously look at the complex interactions between victims and their multiple types of enemies; the ones that do exist focus on a limited set of study systems (Buck et al., 2018). Trends Ecol. Where is the current position of LOMBOK STRAIT presently? Now recognized as a non-consumptive effect, the ecological and evolutionary impact of fear has been studied in a number of predator-prey systems within the last few decades. Therefore, even if growing big reduces the probability of being attacked by a lethal enemy, larger victims may still invest energy in avoidance behaviors against smaller, non-lethal ones. [8] The cultivable marine hydrocarbonoclastic bacteria identified in the Lombok Strait specifically have six morphologies: LS-3, LS-13, LS-14, LS-15, LS-16, and LS-20. doi: 10.1111/1365-2656.12885, Strauss, A. T., Hite, J. L., Civitello, D. J., Shocket, M. S., Caceres, C. E., and Hall, S. R. (2019). The tide in the Lombok Strait is produced by tidal waves propagating from the Indian Ocean with a dominant M 2 semi-diurnal period of 12.4 h. The tidal flow can reach 3.5 m s-1 in the sill area (Murray and Arief, 1988).Numerical simulations have shown a strong conversion of semidiurnal M 2 barotropic to baroclinic internal tides around the NPS (Nagai and Hibiya, 2015; Nugroho et al., 2018 . J-FD wrote the manuscript. Anim. [11], The Indonesian Throughflow (ITF) affects the climate of the region as it regulates the position of hot pools in the Indian Ocean.