Large- and Medium-Sized Land Mammals of Northeast Marajó Island, Lower Amazon, Brazil

Marajó, located in the lower Amazon, Brazil, is one of the largest river islands in the world. Most of the island is subject to tidal or seasonal flooding. Despite its historical, cultural and geographical importance, Marajó Island remains relatively less investigated in terms of mammal diversity, ecology and community structure than the rest of the Amazon. This scenario has motivated the presentation of this list of land mammals of eastern Marajó Island. Two field surveys were conducted in the course of 7-11 December 2012 and 17-25 October 2013 in Jaranduba, Dunas and Ribanceira Farms, northeast portions of Marajó Island. A total of 23 large and medium-sized land mammal species were recorded in the study area. These farms host a representative mammal community of northeastern Marajó, an area lacking previous faunal studies. Human pressure over centuries has deeply modified the environment in Marajó. Therefore, striking evidence of a long human-populated past in this island is in accordance to many other sites throughout the Amazon plain. The result of a land mammal survey in northeastern Marajó is a clear evidence of past and present human interference in the island. Even though Marajó Island has exalted mammal diversity, it will be much higher if long-term studies are effectively implemented.


Introduction
Bordering nearly 49,000 square kilometers, Marajó is one of the largest river islands in the world.Most of the island is subject to tidal or seasonal flooding [1].The local climate can be characterized by two categories: humid tropical, with mean precipitation in the driest month at least 60 mm, and tropical monsoon, with excessive rainfall between January and June.During this period, two thirds of the island is completely flooded [2]- [5].The annual precipitation ranges between 2500 mm and 4000 mm, with a mean temperature of around 27˚C, and relative humidity bordering on 80%.Rainfall is distributed in two distinct periods, with a pronounced rainy season between December and June, and a dry season between July and November.Despite this rigorous hydrological regime, the vegetation which occupies about 40% of the island is flooded annually and is referred to as a savanna or flooded grassland [1]- [9].
Long-term interaction between human societies and the environment has found a prodigal field study in Marajó Island [7].As previously reported, the history of human occupation of the island dates from about 5000 years before present, showing a long background, up to the present, of aquatic resource management [5]- [7].Seasonally, flooded savannas as a natural fish nursery were from time to time and successfully managed in order to feed indigenous and subsequently early settlers [5]- [7].The peak of the fishing economy occurred during an archaeological period known as the Marajoara Phase (400-1350 AD), which featured archaeologically known societies that built mounds and dams as part of efficient hydraulic systems, with the underlying purpose of controlling aquatic fauna and water supplies [7].Such systems, altered during centuries of manipulation, have persisted to the present, even if they have been affected negatively by the interference of cattle, buffalo and horse ranching [4]- [9].
Despite its historical, cultural and geographical importance, Marajó Island remains relatively less investigated in terms of mammal diversity, ecology and community structure than the rest of the Amazon.Early investigations were carried out by naturalists at the end of the 19th century and the beginning of the 20th century [10].There has been an effort to collect in the region in the last decades and specimens have been deposited in the mammals' collection of Museu Nacional, Rio de Janeiro and Museu Paraense Emílio Goeldi, in Belém.Despite such efforts, only in the last decade some mammal species have been recorded for the first time in the Marajó Island.Still, some unresolved questions on the occurrence of two primate species [11] [12] and two cervids [11] [13]- [15] remain.
It is remarkable that Marajó Island, specifically its northeast portion and coastline, has been scarcely surveyed in terms of mammal diversity.Hence, faunal inventories in this particular section of the island are sparse, and are mostly restricted to primates and bats [16]- [26].This scenario has motivated the presentation of this list of land mammals of eastern Marajó Island.

Methods
We conducted two field surveys in the course of 7-11 December 2012 and 17-25 October 2013 to Jaranduba Farm (0˚15'10.20"S;048˚43'06.34"W),located on the municipality of Soure, northeast portion of Marajó Island, lower Amazon, Brazil (Figure 1).As both trips were conducted during dry season, unpaved roads and trails could be crossed by a four-wheel vehicle or by foot (Figure 2).Nearby Dunas (0˚14'33.47"S;048˚45'27.06"W)and Ribanceira Farms (0˚14' 58.09"S; 048˚39'13.48"W)were also visited in search of wild mammal documentation using cameras and recovering carcasses.In addition, a series of interviews were made with native people, born and raised in the area.Information on wild mammal occurrence, habitats and peculiarities was asked to experienced ranchers and former hunters.It should be mentioned that interviews were made spontaneously and relaxed.Only the most reliable answers were selected and double-checked in the second trip.A total of 12 high-quality accounts were accepted and provided the very first checklist of land mammals of northeast Marajó Island.Thus, the list presented here combines voucher specimens deposited in the Museu Paraense Emílio Goeldi (MPEG), cross-checked with citations in historical and current literature, in addition to folk information.

Results
A total of 23 large and medium-sized land mammal species were recorded in the study area.Table 1 lists specimens recovered and deposited in the MPEG mammal collection along with supporting literature for their general occurrence in Marajó Island.An additional list is presented and includes folk documentation of mammal attributes and other conspicuous information as provided by interviewed residents (Table 2).Brief information on the voucher specimens assembled during our expeditions and deposited in MPEG is presented as follows:

Dasypus septemcinctus
Smaller than the other, walk along the night

Tamandua tetradactyla
They can be found in the "tesos"

Alouatta belzebul
They are very noisy

Aotus infulatus
Certain time I shot one thinking it was something else

Cerdocyon thous
It is like a fox, very smart, nocturnal

Nasua nasua
Like to live in the "teso".Quati-mundé is the old male, solitary

Procyon cancrivorus
Live usually close to the water

Lontra longicaudis
Occurs in the igarapé do Siriri, Jaranduba Farm Pteronura brasiliensis I have seen one far away, on the way to Dunas Farm (Jaranduba)

Panthera onca
It is rare around here

Mazama americana
Once they were very abundant

Ozotoceros bezoarticus
Occurs in the fields during high waters, has a white tail Proechimys sp.Lives in trees: "dá trepado".Fur is very red: "pelagem bem vermelha"

Hydrochoerus hydrochaeris
Lives only in the fields (Retiro Caju, Jaranduba).I take care of one newborn that was abandoned by its mother (Retiro São Geraldo, Ribanceira)

Dasyprocta leporina
It is very yellowish in color Common Opossum (Didelphis marsupialis): one skull found on a sandy beach in Ribanceira Farm on 9 December 2012.The presence of "mucuras" was reported in all visited sites.
Nine-banded armadillo (Dasypus novemcinctus): three specimens of nine-banded armadillo (Dasypus novemcinctus) were found in Jaranduba Farm on 10 and 11 December 2012.Armadillos were reported to be fairly common in all sites visited.
Squirrel monkey (Saimiri collinsi): a fairly common species in the "tesos" and along the coastal stretch of vegetation in Jaranduba and Ribanceira Farms.In October 2013, large groups of squirrel monkeys of up to 20 -25 individuals were sighted in Ribanceira Farm hanging on mango trees.Saimiri collinsi is a primate species just recently revalidated [24] [25].
Crab-eating fox (Cerdocyon thous): a pair of crab-eating foxes was sighted on 10 December 2012 at nightfall while returning from Mocambo Farm.On 11 December 2012 a carcass was found on the road to Retiro Pindoba and saved as reference material.We consider these records of particular interest as little is known on the biogeography and ecology of crab-eating fox in Marajó Island and eastern Amazon in general [27] [28].
Capybara (Hydrochoerus hydrochaeris): the capybara is the largest living rodent, with adults weighing 49 -50 kg (range 35 -65) [29].This large mammal has long been reported to inhabit the grasslands of Marajó Island [10] [30] [31].Indeed, capybaras were commonly sighted during the two field campaigns.Not surprisingly, carcasses were easily found and skulls were collected on both expeditions (Figure 2).A severe drought and salinization of the fields was observed in the 2012 field campaign.According to locals, by the end of the dry season, capybaras were forced to drink salted water, soon became weak and many perished.We noted several emaciated capybaras and some seemed to be roaming in the fields in search of water or a wetter location.A captive small capybara was found in Ribanceira Farm in October 2013 (Figure 3).

Discussion
Humans have occupied Marajó Island for at least the past five to seven thousand years [32] [33].These first inhabitants probably subsisted on fish and game hunting and small-scale agriculture [7].It has been generally reported that cultivation would have been limited in recent times by the low fertility of the land and their inadequate drainage [5]- [7].As early as the Seventieth Century cattle ranching has spread out in the fields of Marajó and has since grown to over a million cows and water buffaloes and one hundred thousand horses by 1990 [34] [35].This immense herd causes severe impacts on the soil and the environment by consequence [34]- [39].
In effect, during our expeditions, domestic pigs, along with cattle, buffaloes, horses and mules, were the most commonly sighted large mammals in the grasslands of Marajó Island.While buffaloes were usually confined to remaining pools (Figure 4), pigs, in contrast, seem to do well during the dry season.Piglets were found elsewhere, often approaching the houses in search of extra food, indicating reproduction success even at this time of year.Domestic dogs (Canis lupus familiaris) are used to protect houses from invading pigs.Related to this, domestic cats (Felis catus) are used to catch mice and bats.
As pointed out by early authors [5] [6], the weight of water buffaloes results in hoofprints of up to 10 cm in depth [40] which, together with their habit of excavating holes in which they cool themselves during the dry season, provoke significant alterations in the structure of the superficial soil layers and the composition of the vegetation, which favor erosive processes [41].The compact soil, hardened in the scorching sun, creates an environment unfavorable for plant growth, thus reducing the productivity and longevity of forage species [42].This is the so called "aterroada", the local designation of the "caboclos" ranchers for such particular condition of the soil.By contrast, in beginning of the rainy season, the aterroada soon become soaked in heavy rain, and cattle have to move to elevated parts.The primitive people of Marajó has learned how to use this condition in favor, creating the "tesos" or "mounds", that could reach 200 m in length, 30 m wide and 10 m in height [43].The landscape of Jaranduba Farm is a classical combination of aterroadas and tesos, the latter dominated by palms (Astrocaryum vulgare) and cashew trees (Anacardium occidentale).Squirrel monkeys (Saimiri collinsi), capybaras (Hydrochoerus hydrochaeris) and coatis (Nasua nasua) (Figure 5) were observed using the tesos habitat for  foraging and shading from sun.Guariba monkeys (Alouatta belzebul) prefer the taller trees, which are usually found closer the coastline.Agoutis (Dasyprocta cf.croconota) were also seen amid the coastal vegetation, as mixture of forest, shrub and planted trees dominate.It is worth saying that our results coincide with a previous survey conducted in 1988 that only reported two primate species (S. collinsi and A. belzebul) in a similar environment in the northeast of Marajó Island [17].
In this sense, the combination of extreme environments, peculiarly compressed soils in the dry season, in contrast to flooded and unstable in the rainy season, is selective for establishment of some wild mammals.This could explain the absence of sloths (Bradypus variegatus and Choloepus didactylus) on Jaranduba and Ribanceira Farms, decidedly cited by locals as non-occurring in the area (In Portuguese: "aqui não tem"), as well as small cats, skunks and some marsupials.
The mammal community of eastern Marajó Island is naturally a result of human pressure directed to every available possibility of use.This includes hunting, practiced for centuries in Marajó Island [22]- [25] as a precondition of daily food income in farms and villages or to be exported as "meat" to Belém.This certainly has been the major cause of decline of the number of many mammal species, including other large desired targets, as caimans and turtles [34] [35].As such, hunting could be credited as the main reason of local extinctions of peccaries, tapirs and pumas and the decrease of jaguars.As a matter of fact, jaguars and pumas were intensively hunted in Marajó Island, as they are seen as natural killers of cattle [35].
The Marajó archipelago has been designated as a state conservation unit in 1989, covering 5,500,000 square kilometers [44].Although the Marajó Island has gained this status, it has been postulated that little has been done to advance environmental protection on Marajó archipelago [6].
As mentioned before, most of the eastern part of the island is used for cattle and water buffalo ranching, and the western forests are being heavily logged.Altogether, human pressure over centuries has deeply modified the environment in Marajó Island.Therefore, striking evidence of a long human-populated past in Marajó is in accordance to many other sites throughout the Amazon plain [45].The result of a land mammal survey in northeastern Marajó is a clear evidence of past and present human interference in the island.Even though, there exist exalted mammal diversity in Marajó Island and, of course, it will be much higher if long-term studies are effectively implemented.

Conclusion
The northeastern Marajó Island, notably Jaranduba, Dunas and Ribanceira Farms, hosts a representative mammal community, an area lacking previous faunal studies.Our surveys have cataloged a total of 23 large-and medium-sized land mammal species in the study area.We have reached a factual report of long-term presence of men in Marajó Island and its consequent mammal community.

Figure 2 .
Figure 2. Carcass of a capybara (Hydrochoerus hydrochaeris) found in Jaranduba farm, Marajó Island, Pará, Brazil, in October 2013.Note the dry vegetation on the back and soil condition.Photo by Rodrigo Baleia.

Figure 4 .
Figure 4. Water Buffaloes cooling in a mud pool during dry season in Jaranduba Farm, Marajó Island, Pará, Brazil.Note the Marajó "tesos" or mounds on the back.Photo by Rodrigo Baleia.

Figure 5 .
Figure 5.South American Coati (Nasua nasua) visiting mango trees nearby the big house of Jaranduba Farm in October, 2013.Photo by Rodrigo Baleia.

Table 1 .
List of large and medium sized mammal specimens recovered during expeditions to Jaranduba, Dunas and Ribanceira Farms in 2012 and 2013, deposited in the Museu Paraense Emílio Goeldi collection, along with supporting literature for their general occurrence in Marajó Island, Brazil.

Table 2 .
Folk information on the occurrence of land mammals in Jaranduba, Dunas and Ribanceira Farms, Eastern Marajó Island, Brazil.