Science for a wilder Anthropocene: Synthesis and future directions for trophic rewilding research.

Trophic rewilding is an ecological restoration strategy that uses species introductions to restore top-down trophic interactions and associated trophic cascades to promote self-regulating biodiverse ecosystems. Given the importance of large animals in trophic cascades and their widespread losses and resulting trophic downgrading, it often focuses on restoring functional megafaunas. Trophic rewilding is increasingly being implemented for conservation, but remains controversial. Here, we provide a synthesis of its current scientific basis, highlighting trophic cascades as the key conceptual framework, discussing the main lessons learned from ongoing rewilding projects, systematically reviewing the current literature, and highlighting unintentional rewilding and spontaneous wildlife comebacks as underused sources of information. Together, these lines of evidence show that trophic cascades may be restored via species reintroductions and ecological replacements. It is clear, however, that megafauna effects may be affected by poorly understood trophic complexity effects and interactions with landscape settings, human activities, and other factors. Unfortunately, empirical research on trophic rewilding is still rare, fragmented, and geographically biased, with the literature dominated by essays and opinion pieces. We highlight the need for applied programs to include hypothesis testing and science-based monitoring, and outline priorities for future research, notably assessing the role of trophic complexity, interplay with landscape settings, land use, and climate change, as well as developing the global scope for rewilding and tools to optimize benefits and reduce human-wildlife conflicts. Finally, we recommend developing a decision framework for species selection, building on functional and phylogenetic information and with attention to the potential contribution from synthetic biology.

Evaluation of artificial heating sources for the thermoregulation of Aldabra giant tortoises (Aldabrachelys gigantea) in Zurich zoo.

We recorded the thermoregulatory patterns of five Aldabra giant tortoises (Aldabrachelys gigantea) (25-193 kg) during spring (ZRH spring trial), after the installation of a heating area (concrete heat pad and basking lamp) at Zurich Zoo, Switzerland. The measurements were compared to published results on the same tortoises observed prior to the installation of the heater (ZRH summer and winter trials), and on wild tortoises on Aldabra Atoll. The mean environmental temperature outside the heating area was 23.3 °C, significantly lower compared to Aldabra Atoll (30.3 °C; range: 23.8-43.8 °C), and to the environmental temperature range at which tortoises maximize their activity in the wild (Ta-opt ; 25.8-31.7 °C). The heating area exhibited a mean temperature of 36.3 °C, and tortoises that made use of the heating area were able to maintain a mean core body temperature (Tbc ) of 30.0 °C, which was comparable to the Tbc of tortoises during ZRH summer and on Aldabra trials, and an improvement over the mean Tbc recorded during the ZRH winter trial (21.2 °C). The smaller individuals reached the upper limits of Tbc recommended for the species, probably due to heating pad temperatures above Ta-opt . We discuss current practices to provide external heating sources for tortoises and how this method can be used to provide an adequate thermal environment for large captive reptiles. Finally, we provide recommendations for the installation of artificial heating sources for tortoises and large reptiles.

Floral signposts: testing the significance of visual 'nectar guides' for pollinator behaviour and plant fitness.

Nectar guides, contrasting patterns on flowers that supposedly direct pollinators towards a concealed nectar reward, are taxonomically widespread. However, there have been few studies of their functional significance and effects on plant fitness. Most previous studies focused on pollinator behaviour and used artificial flowers in laboratory settings. We experimentally investigated the role of putative nectar guides in a natural system: the South African iris Lapeirousia oreogena, whose flowers have a clearly visible pattern of six white arrow-markings pointing towards the narrow entrance of the long corolla tube, and its sole pollinator, a long-proboscid nemestrinid fly. We painted over none, some or all of the white arrow-markings with ink that matched the colour of the corolla background. Although arrow-marking removal had little effect on the approaches by flies to flowers from a distance, it dramatically reduced the likelihood of proboscis insertion. Export of pollen dye analogue (an estimate of male fitness) was reduced to almost zero in flowers from which all nectar guides had been removed, and fruit set (a measure of female fitness) was also significantly reduced. Our results confirm that the markings on L. oreogena flowers serve as nectar guides and suggest that they are under strong selective maintenance through both male and female fitness components in this pollination system.

Carrion mimicry in a South African orchid: flowers attract a narrow subset of the fly assemblage on animal carcasses.

BACKGROUND AND AIMS: Although pollination of plants that attract flies by resembling their carrion brood and food sites has been reported in several angiosperm families, there has been very little work done on the level of specificity in carrion mimicry systems and the importance of plant cues in mediating such specialization. Specificity may be expected, as carrion-frequenting flies often exploit different niches, which has been interpreted as avoidance of interspecific competition. Interactions between the orchid Satyrium pumilum and a local assemblage of carrion flies were investigated, and the functional significance of floral traits, especially scent, tested. Pollination success and the incidence of pollinator-mediated self-pollination were measured and these were compared with values for orchids with sexual- and food-deceptive pollination systems. METHODS AND KEY RESULTS: Observations of insect visitation to animal carcasses and to flowers showed that the local assemblage of carrion flies was dominated by blow flies (Calliphoridae), house flies (Muscidae) and flesh flies (Sarcophagidae), but flowers of the orchid were pollinated exclusively by flesh flies, with a strong bias towards females that sometimes deposited live larvae on flowers. A trend towards similar partitioning of fly taxa was found in an experiment that tested the effect of large versus small carrion quantities on fly attraction. GC-MS analysis showed that floral scent is dominated by oligosulfides, 2-heptanone, p-cresol and indole, compounds that also dominate carrion scent. Flesh flies did not distinguish between floral and carrion scent in a choice experiment using olfactory cues only, which also showed that scent alone is responsible for fly attraction. Pollination success was relatively high (31·5 % of flowers), but tracking of stained pollinia also revealed that a relatively high percentage (46 %) of pollen deposited on stigmas originates from the same plant. CONCLUSIONS: Satyrium pumilum selectively attracts flesh flies, probably because its relatively weak scent resembles that of the small carrion on which these flies predominate. In this way, the plants exploit a specific subset of the insect assemblage associated with carrion. Pollination rates and levels of self-pollination were high compared with those in other deceptive orchids and it is therefore unlikely that this mimicry system evolved to promote outcrossing.

Frugivory and seed dispersal by chelonians: a review and synthesis.

In recent years, it has become clear that frugivory and seed dispersal (FSD) by turtles and tortoises is much more common than previously thought. We here review published and unpublished records of chelonian FSD, and assess the role of chelonians as seed dispersers, from individual species to the community level. We first discuss the distribution of chelonian FSD and the characteristics of the fruit and/or seed species eaten and dispersed by chelonians. We then use the seed dispersal efficiency framework to explore the quantitative and qualitative components of seed dispersal by tortoises and turtles, embarking on a journey from when the fruits and/or seeds are consumed, to when and where they are deposited, and assess how efficient chelonians are as seed dispersers. We finally discuss chelonian FSD in the context of communities and of chelonians as megafauna. A substantial proportion of the world's aquatic and terrestrial turtles and a major part of testudinid tortoises (71 species in 12 families) include fruits and/or seeds in their diet; fruits of at least 588 plant species in 121 families are ingested and/or dispersed by chelonians. For some chelonians, overall or in certain seasons, fruit may even form the largest part of their diet. Contrary to seed dispersal by lizards, the other major reptilian frugivores, chelonian FSD is not an island phenomenon in terms of geographic distribution. Nevertheless, on islands tortoises are often among the largest native terrestrial vertebrates - or were until humans arrived. We synthesise our knowledge of chelonian FSD, and discuss the relevance of our findings for conservation and restoration, especially in relation to rewilding with large and giant tortoises.

Island rewilding with giant tortoises in an era of climate change.

Replacing recently extinct endemic giant tortoises with extant, functional analogues provide the perhaps best examples of island rewilding to date. Yet, an efficient future application of this conservation action is challenging in an era of climate change. We here present and discuss a conceptual framework that can serve as a roadmap for the study and application of tortoise rewilding in an uncertain future. We focus on three main ecological functions mediated by giant tortoises, namely herbivory, seed dispersal and nutrient cycling, and discuss how climate change is likely to impact these. We then propose and discuss mitigation strategies such as artificial constructed shade sites and water holes that can help drive and maintain the ecosystem functions provided by the tortoises on a landscape scale. The application of the framework and the mitigation strategies are illustrated with examples from both wild and rewilded populations of the Aldabra giant tortoise, Aldabrachelys gigantea, in the Western Indian Ocean.This article is part of the theme issue 'Trophic rewilding: consequences for ecosystems under global change'.

Trophic interactions between larger crocodylians and giant tortoises on Aldabra Atoll, Western Indian Ocean, during the Late Pleistocene.

Today, the UNESCO World Heritage Site of Aldabra Atoll is home to about 100 000 giant tortoises, Aldabrachelys gigantea, whose fossil record goes back to the Late Pleistocene. New Late Pleistocene fossils (age ca. 90-125 000 years) from the atoll revealed some appendicular bones and numerous shell fragments of giant tortoises and cranial and postcranial elements of crocodylians. Several tortoise bones show circular holes, pits and scratch marks that are interpreted as bite marks of crocodylians. The presence of a Late Pleistocene crocodylian species, Aldabrachampsus dilophus, has been known for some time, but the recently found crocodylian remains presented herein are distinctly larger than those previously described. This indicates the presence of at least some larger crocodylians, either of the same or of a different species, on the atoll. These larger crocodylians, likely the apex predators in the Aldabra ecosystem at the time, were well capable of inflicting damage on even very large giant tortoises. We thus propose an extinct predator-prey interaction between crocodylians and giant tortoises during the Late Pleistocene, when both groups were living sympatrically on Aldabra, and we discuss scenarios for the crocodylians directly attacking the tortoises or scavenging on recently deceased animals.

Patterns of activity and body temperature of Aldabra giant tortoises in relation to environmental temperature.

We studied the temperature relations of wild and zoo Aldabra giant tortoises (Aldabrachelys gigantea) focusing on (1) the relationship between environmental temperature and tortoise activity patterns (n = 8 wild individuals) and (2) on tortoise body temperature fluctuations, including how their core and external body temperatures vary in relation to different environmental temperature ranges (seasons; n = 4 wild and n = 5 zoo individuals). In addition, we surveyed the literature to review the effect of body mass on core body temperature range in relation to environmental temperature in the Testudinidae. Diurnal activity of tortoises was bimodally distributed and influenced by environmental temperature and season. The mean air temperature at which activity is maximized was 27.9°C, with a range of 25.8-31.7°C. Furthermore, air temperature explained changes in the core body temperature better than did mass, and only during the coldest trial, did tortoises with higher mass show more stable temperatures. Our results, together with the overall Testudinidae overview, suggest that, once variation in environmental temperature has been taken into account, there is little effect of mass on the temperature stability of tortoises. Moreover, the presence of thermal inertia in an individual tortoise depends on the environmental temperatures, and we found no evidence for inertial homeothermy. Finally, patterns of core and external body temperatures in comparison with environmental temperatures suggest that Aldabra giant tortoises act as mixed conformer-regulators. Our study provides a baseline to manage the thermal environment of wild and rewilded populations of an important island ecosystem engineer species in an era of climate change.

Positive indirect interactions between neighboring plant species via a lizard pollinator.

In natural communities, species are embedded in networks of direct and indirect interactions. Most studies on indirect interactions have focused on how they affect predator-prey or competitive relationships. However, it is equally likely that indirect interactions play an important structuring role in mutualistic relationships in a natural community. We demonstrate experimentally that on a small spatial scale, dense thickets of endemic Pandanus plants have a strong positive trait-mediated indirect effect on the reproduction of the declining endemic Mauritian plant Trochetia blackburniana. This effect is mediated by the endemic gecko Phelsuma cepediana moving between Pandanus thickets, a preferred microhabitat, and nearby T. blackburniana plants, where it feeds on nectar and pollinates the plants. Our findings emphasize the importance of considering plant-animal interactions such as pollination at relatively small spatial scales in both basic ecological studies and applied conservation management.

Decline in abundance and health state of an Atlantic subtropical gorgonian population.

Losses in coral cover have been widely reported for the Caribbean. In contrast, much less is known about the health state of the Brazilian reef fauna, which was declared as a priority for Atlantic biodiversity conservation due to its high degree of endemism. In the present study, we assessed the general health state of Phyllogorgia dilatata assemblages at the subtropical reefs of Arraial do Cabo (southeastern Brazil), where observations suggest that the abundance of this endemic gorgonian species has declined. We found that about 49% of the sampled colonies were dead, and 73% of the living colonies were affected by tissue loss. Tissue loss initially manifested as multifocal holes in the planar colonial coenenchyme and peripheral tissue retraction leaving denuded skeletal axes. In combination with other recent studies, our results raise the awareness for an increasingly threatened Southwestern Atlantic reef coral fauna.

Non-native megaherbivores: the case for novel function to manage plant invasions on islands.

There is a heated debate about whether all non-native species are 'guilty until proven innocent', or whether some should be accepted or even welcomed. Further fanning the flames, I here present a case where introductions of carefully vetted, non-native species could provide a net conservation benefit. On many islands, native megaherbivores (flightless birds, tortoises) recently went extinct. Here, rewilding with carefully selected non-native species as ecological replacements is increasingly considered a solution, reinstating a herbivory regime that largely benefits the native flora. Based on these efforts, I suggest that restoration practitioners working on islands without a history of native megaherbivores that are threatened by invasive plants should consider introducing a non-native island megaherbivore, and that large and giant tortoises are ideal candidates. Such tortoises would be equally useful on islands where eradication of invasive mammals has led to increased problems with invasive plants, or on islands that never had introduced mammalian herbivores, but where invasive plants are a problem. My proposal may seem radical, but the reversibility of using giant tortoises means that nothing is lost from trying, and that indeed much is to be gained. As an easily regulated adaptive management tool, it represents an innovative, hypothesis-driven 'innocent until proven guilty' approach.

Persistence of distinctive morphotypes in the native range of the CITES-listed Aldabra giant tortoise.

Understanding the extent of morphological variation in the wild population of Aldabra giant tortoises is important for conservation, as morphological variation in captive populations has been interpreted as evidence for lingering genes from extinct tortoise lineages. If true, this could impact reintroduction programmes in the region. The population of giant tortoises on Aldabra Atoll is subdivided and distributed around several islands. Although pronounced morphological variation was recorded in the late 1960s, it was thought to be a temporary phenomenon. Early researchers also raised concerns over the future of the population, which was perceived to have exceeded its carrying capacity. We analyzed monthly monitoring data from 12 transects spanning a recent 15-year period (1998-2012) during which animals from four subpopulations were counted, measured, and sexed. In addition, we analyzed survival data from individuals first tagged during the early 1970s. The population is stable with no sign of significant decline. Subpopulations differ in density, but these differences are mostly due to differences in the prevailing vegetation type. However, subpopulations differ greatly in both the size of animals and the degree of sexual dimorphism. Comparisons with historical data reveal that phenotypic differences among the subpopulations of tortoises on Aldabra have been apparent for the last 50 years with no sign of diminishing. We conclude that the giant tortoise population on Aldabra is subject to varying ecological selection pressures, giving rise to stable morphotypes in discrete subpopulations. We suggest therefore that (1) the presence of morphological differences among captive Aldabra tortoises does not alone provide convincing evidence of genes from other extinct species; and (2) Aldabra serves as an important example of how conservation and management in situ can add to the scientific value of populations and perhaps enable them to better adapt to future ecological pressures.

Resurrecting extinct interactions with extant substitutes.

There is increasing evidence that restoration ecologists should be most concerned with restoring species interactions rather than species diversity per se [1]. Rewilding with taxon substitutes, the intentional introduction of exotic species to replace the ecosystem functions of recently extinct species, is one way to reverse ecosystem dysfunction following the loss of species interactions [2]. This is highly controversial [3], in part because of a lack of rigorous scientific studies [4]. Here we present the first empirical evidence of an in situ rewilding project undertaken as a hypothesis-driven ecosystem management option. On Ile aux Aigrettes, a 25-hectare island off Mauritius, the critically endangered large-fruited endemic ebony, Diospyros egrettarum (Ebenaceae), was seed-dispersal limited after the extinction of all native large-bodied frugivores, including giant tortoises. We introduced exotic Aldabra giant tortoises, Aldabrachelys gigantea, to disperse the ebony seeds. Not only did the tortoises ingest the large fruits and disperse substantial numbers of ebony seeds, but tortoise gut passage also improved seed germination, leading to the widespread, successful establishment of new ebony seedlings. Our results demonstrate that the introduction of these exotic frugivores is aiding the recovery of ebonies. We argue for more reversible rewilding experiments to investigate whether extinct species interactions can be restored.

Seed dispersal and establishment of endangered plants on Oceanic Islands: the Janzen-Connell model, and the use of ecological analogues.

BACKGROUND: The Janzen-Connell model states that plant-specific natural enemies may have a disproportionately large negative effect on progeny close to maternal trees. The majority of experimental and theoretical studies addressing the Janzen-Connell model have explored how it can explain existing patterns of species diversity in tropical mainland areas. Very few studies have investigated how the model's predictions apply to isolated oceanic islands, or to the conservation management of endangered plants. Here, we provide the first experimental investigation of the predictions of the Janzen-Connell model on an oceanic island, in a conservation context. In addition, we experimentally evaluate the use of ecological analogue animals to resurrect the functional component of extinct frugivores that could have dispersed seeds away from maternal trees. METHODOLOGY/PRINCIPAL FINDINGS: In Mauritius, we investigated seed germination and seedling survival patterns of the critically endangered endemic plant Syzygium mamillatum (Myrtaceae) in relation to proximity to maternal trees. We found strong negative effects of proximity to maternal trees on growth and survival of seedlings. We successfully used giant Aldabran tortoises as ecological analogues for extinct Mauritian frugivores. Effects of gut-passage were negative at the seed germination stage, but seedlings from gut-passed seeds grew taller, had more leaves, and suffered less damage from natural enemies than any of the other seedlings. CONCLUSIONS/SIGNIFICANCE: We provide the first experimental evidence of a distance-dependent Janzen-Connell effect on an oceanic island. Our results potentially have serious implications for the conservation management of rare plant species on oceanic islands, which harbour a disproportionately large fraction of the world's endemic and endangered plants. Furthermore, in contrast to recent controversy about the use of non-indigenous extant megafauna for re-wilding projects in North America and elsewhere, we argue that Mauritius and other oceanic islands are ideal study systems in which to empirically explore the use of ecological analogue species in restoration ecology.

Coloured nectar: distribution, ecology, and evolution of an enigmatic floral trait.

While coloured nectar has been known to science at least since 1785, it has only recently received focused scientific attention. However, information about this rare floral trait is scattered and hard to find. Here, we document coloured nectar in 67 taxa worldwide, with a wide taxonomical and geographical distribution. We summarise what is currently known about coloured nectar in each of the lineages where it occurs. The most common nectar colours are in the spectrum from yellow to red, but also brown, black, green, and blue colours are found. Colour intensity of the nectar varies, sometimes even within one taxa, as does the level of contrast between flower petals and nectar. Coloured nectar has evolved independently throughout the angiosperms at least 15 times at the level of family, and is in many cases correlated with one or more of three parameters: (1) vertebrate pollination, known or hypothesised, (2) insularity -- many species are from islands or insular mainland habitats, and (3) altitude -- many species are found at relatively high altitudes. We discuss the evolution and speculate on possible ecological functions of coloured nectar. Apart from being a non-functional, perhaps pleiotropic, trait, we present several hypotheses on possible ecological functions of coloured nectar. Firstly, for some plant species it can be interpreted as an honest signal, leading to high pollination efficiency. Secondly, it can function as a deterrent against nectar-thieves or inefficient pollinators, thus acting as a floral filter. Thirdly, nectar colour-pigments can have anti-microbial qualities that may protect the nectar in long-lived flowers. Neither of these possibilities are mutually exclusive. Recent studies have provided experimental evidence for the first two hypotheses, and we suggest promising avenues for future research into this little-known floral trait.

Mauritian coloured nectar no longer a mystery: a visual signal for lizard pollinators.

Most floral nectars are clear as water, and the enigmatic coloured nectar in three endemic plant species in Mauritius has puzzled scientists studying it. One hypothesis about the possible ecological function of coloured nectar is that it serves as a visual signal for pollinators. Recent studies have shown that at least two of the three Mauritian plant species with coloured nectar are visited and pollinated by endemic Phelsuma geckos. We here provide experimental evidence for the visual signal hypothesis by showing that Phelsuma ornata geckos prefer coloured over clear nectar in artificial flowers. In flowering plants, coloured nectar could additionally function as an honest signal that allows pollinators to assert the presence and judge the size of a reward prior to flower visitation, and to adjust their behaviour accordingly, leading to increased pollinator efficiency. Our study provides a first step in understanding this rare and intriguing floral trait.