These records may have been previously overlooked because the word mangrove was not mentioned in the title, abstract, or keywords of the papers in question, and so may not have been picked up by search engines. The survey generated responses from 59 individuals including positive reports from 15 respondents relating to observations of 22 species; of these, at least 9 species have not previously been reported from mangrove habitats. Five records were supported by photographs Fig. Of the records that can be assigned to species on the basis of locality, 20 species are globally threatened with extinction, of which 3 are Vulnerable, 13 Endangered, and 4 Critically Endangered Schwitzer et al.
One additional species was reported by local staff of the Eden Reforestation Project and matches the description of Cheirogaleus medius , but I treat this record as unconfirmed because it was reported second hand and thus do not include it in the species totals. Images of lemurs in mangroves provided by survey respondents. Neither published records nor survey respondents tended to provide much information with regard to the behavior of observed lemurs within mangrove habitats, at least in part because observations were generally brief, one-off events, and the fact that it may be difficult to ascribe behavior categories to active individuals at night.
Nevertheless, the reports indicate that different species may use mangroves for a variety of reasons including shelter, moving between patches of terrestrial habitat, and procuring food or water. In terms of shelter, two nocturnal species, Microcebus cf. Andriamahanina and F. Razafindrajao pers. Shattenberg pers. The diurnal Eulemur rufus and Propithecus coronatus use mangroves as sleeping sites Gauthier et al.
Tarnaud and R. Ramanamisata pers. Mbohoahy pers. As well as resting and sleeping sites, mangroves may be used as corridors for travel between patches of terrestrial habitat, e. In terms of foraging and food resources, C.
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Borgerson pers. Heritiera littoralis , L.
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Razafitsalama pers. Randrianjohany pers. Mangroves have also been reported as a feeding site for Propithecus coronatus and Eulemur mongoz Gauthier et al. Among nocturnal species, S. Wolf pers. Ferguson has observed 5—10 Microcebus cf. Ferguson pers. On Mayotte Comoros archipelago the introduced Eulemur fulvus uses mangrove areas to seemingly supplement its diet with minerals; L. In the latter instance, the observer believed that the lemurs may be licking dew as well as salt accreted from the leaves L. Tarnaud pers.
Finally, Lemur catta drinks water from freshwater seeps within mangroves in semi-arid areas of far southern Madagascar Sauther et al. Observations of Propithecus coquereli and Microcebus cf. Gardner and L. Jasper unpubl. Few data are available on the seasonality of mangrove use, though reported observations show no clear patterns in temporal variation. Some species have been reported from mangroves at the same site in both wet and dry seasons, e. Mangroves present a challenging environment for primates as a result of their frequent inundation, low botanical and structural diversity, and foliage that tends to be unpalatable because of a high tannin content Kraus et al.
They may also harbor lower invertebrate diversity and biomass than terrestrial forests, though comparative data are scarce Intachat et al. Nevertheless this review has shown that diverse lemur species are able to use mangroves in some circumstances. The published and unpublished observations collected here almost double the number of lemur species known to occur in mangroves and, alongside a recent review Donati et al. They also add a new family Lepilemuridae and two new genera Lepilemur , Mirza to the global list.
Based on a visual interpretation of distribution maps Mittermeier et al. These findings suggest that the facultative use of mangroves is much more widespread among lemurs than was previously thought, though there remains no evidence that any lemurs are obligate or specialist mangrove dwellers.
The lack of specialist mangrove species may be considered surprising given that several lemur species Hapalemur spp. Thus neither the unpalatability nor the regular inundation of mangroves need necessarily have constituted a barrier to the evolution of mangrove use by species in these genera. Lemurs were reported to use mangroves for a variety of reasons, including 1 to rest or sleep in, 2 to rest in the shade during hot parts of the day, 3 to move between patches of forest, 4 to forage on mangrove tree resources fruit, flowers, leaves , 5 to feed on minerals, and 6 to drink water.
Some primarily insectivorous, nocturnal species, e. Microcebus spp. Mangroves may also provide a refuge from predation for some primate species owing to their regular inundation Matsuda et al. Although evidence is lacking, this may also be a factor for some lemurs because nonavian lemur predators, which include Euplerid carnivores, domestic and feral cats and dogs, and a range of snakes Gardner et al. Furthermore, mangroves may provide a refuge from human hunters, who target lemurs through much of Madagascar Borgerson et al.
The extent to which different species use mangroves varies greatly, and some species may occur in this habitat only occasionally or under rare circumstances. For example, Cortni Borgerson pers.
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Bayart and Simmen found only one of three focal groups of Eulemur macaco at Ampasikely to include mangroves within their territory, and only in one of three years, while Chris Birkinshaw pers. Gardner unpubl. For example, mangroves are said to be the preferred habitat of Propithecus coronatus at Antrema Roger and Andrianasolo , and were reported from there by four respondents in this study, while P.
Likewise mangrove use by Lemur catta has been widely reported from south of Toliara Donati et al. ND , though this may be the only area within the range of the species in which mangroves occur. While most observations were made at or close to the edge of mangrove stands this is likely to reflect sampling bias, as their dense growth and regular inundation render mangroves much easier to travel past, on the landward or seaward side, than to travel through.
Past and Present Distributions of Lemurs in Madagascar
Thus these data should not be regarded as evidence that lemurs tend only to use mangrove edge habitats. Indeed, observations of Microcebus cf. Whereas the former were frequently observed in an area where mangroves are contiguous with intact native forest, the adjacent vegetation at Antsahampano where Microcebus cf. The absence of contiguous native forest cover from these areas suggests that the observed populations are not dependent on source-sink dynamics and the immigration of individuals from areas of higher quality habitat Pulliam , but are in fact able to maintain viable populations in the mangrove.
It has been hypothesized or demonstrated that lemurs and other primates may use mangroves as a refuge following loss of, or disturbance to, preferred habitats Galat-Luong and Galat ; Gauthier et al. Although the presence of lemurs in mangroves lacking adjacent terrestrial habitats may be taken as evidence in support of this hypothesis, we cannot infer that mangroves are suboptimal habitat because we do not know whether these species also used mangroves when connecting terrestrial forests remained.
If mangroves do function as refuge habitats for some nocturnal lemurs, the key resource they provide may be daytime sleeping sites. Most species in the Cheirogaleidae and Lepilemuridae spend the day in nests or tree holes Mittermeier et al. Respondents in this study reported several species in these families as sleeping within tree holes, under loose bark, and in hollow branches, often from areas lacking alternative sleeping sites, e.
However, there is some indirect evidence that no lemurs widely use such mangrove refugia. The Madagascar teal Anas bernieri is a mangrove specialist duck that breeds only in tree holes in mature Avicennia marina Young ; Young et al.test23.edge-ai-vision.com/blue-suede-shoes.php
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Suitable nest sites are rare because Madagascar lacks hole-excavating animals such as woodpeckers; thus it has been hypothesized that the teal would not have been able to evolve its breeding habits if it had to compete for tree holes with lemurs G. Young pers. Much further research is required to understand better the role of mangroves in the maintenance of lemur populations.
This is particularly important for a number of mangrove-using species in northwest Madagascar, such as Microcebus mamiratra , M. However, even if mangroves are demonstrated to provide important habitat for these species they may not be more secure than terrestrial forests, as mangrove deforestation rates may match or even exceed those of terrestrial forests in some parts of the region Jones et al. The mixed-methods approach I adopted for this review allowed the collection of numerous published and unpublished observations that together have greatly expanded our knowledge of mangrove use by lemurs.
We now know that more than half of all lemurs with distributions encompassing mangrove areas are able to use them facultatively in some circumstances, and may do so for a number of reasons. However, observations are almost entirely anecdotal so our understanding of the role of mangroves in the maintenance of lemur populations remains extremely limited.
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Given the difficulties of surveying mangroves, camera trap and video technologies may provide useful tools in this regard. Ninety-four percent of all lemur species are threatened with extinction, primarily as a result of ongoing habitat loss Schwitzer et al. This research was carried out within the framework of a mangrove conservation project funded by the Global Environment Facility.
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I also thank Leah Glass for preparation of Fig. Two anonymous reviewers and the editor-in-chief also provided comments that greatly improved the clarity of the manuscript.