The effect of anthropogenic habitat usage on the social behaviour of a vulnerable species, Cyclura nubila

Kathryn E. Lacy1 and Emília P. Martins2
1.Department of Biology, University of Oregon, Eugene, Oregon, 97405, USA; kitlacy@qwest.net
2.Department of Biology, Jordan Hall, Indiana University, Bloomington, Indiana, 47405, USA.

ABSTRACT

With the increasing human population world-wide, animals and humans are sharing more habitat. In this study, we consider the consequences of this habitat usage overlap on the behaviour patterns and social structure of a threatened species. Specifically, we used focal animal samples to collect data on the Cuban rock iguana, Cyclura nubila, in six field sites. Three of these sites are subject to considerable anthropogenic habitat usage, whereas three are in relatively low anthropogenic usage areas. Individuals in high anthropogenic usage sites were more closely assembled, with more males and females sharing a smaller amount of space. These animals exhibited even more aggressive behaviour and social interactions than expected when taking into account the larger number of possible interactants. High anthropogenic usage sites also had more male–male interactions and fewer males interacting with females. We suggest that social and mating system changes have occurred. Ramifications of these recent changes in the behavioural repertoires on the long-term survival of the species are discussed.

DISCUSSION

Our results suggest that significant anthropogenic presence can result in differences not only in the overall density of animals at a site (i.e. the number of nearest neighbours), but also in the behavioural repertoire and social organization of a species in ways that could have considerable impact on the population genetics, demographics and long-term survival of endangered species. Although we cannot distinguish between the direct effects of anthropogenic disturbance (e.g. feeding) and longer-term effects such as the higher animal densities (probably also the result of anthropogenic disturbance), we found several patterns of interest. Cyclura nubila in our high anthropogenic usage sites were found in groups approximately three times bigger than the low anthropogenic usage sites, had more frequent social interactions and higher levels of aggression. More specifically, virtually all males in areas of low human impact interacted regularly with only a single female/ juvenile. In high anthropogenic usage sites, there were several males who interacted with no females at all and a few who regularly interacted with more than four female/juveniles.
Individuals in high anthropogenic usage sites engaged in more frequent aggressive interactions than those in low anthropogenic usage sites. Although some increase in aggression can be explained by the increase in the number of animals, the observed difference was substantially greater than that expected based solely on the concurrent increase in the number of neighbouring individuals (i.e. possible interactants) at high anthropogenic usage sites.
This extends the results of primate crowding studies in which aggression also increased more than expected given the number of animals (e.g. Wrangham, 1974; Hill, 1999).
As with crowded captive green iguanas (Alberts, 1994), a few ‘despotic’ males seem to have emerged at high anthropogenic usage sites. Apparently instead of reducing aggression among male C. nubila, however, frequent aggressive encounters among males persist despite the change in social structure.
Excessive aggression among adult males can lead to greater stress and inhibit the behaviour of smaller animals.
This conclusion is reinforced by the observation of significantly more tongue touching in high anthropogenic usage sites. Tongue touching in lizards is thought to be related to stress commonly associated with exploratory behaviour (e.g., Greenberg 1985, 1993; Burghardt, Allen & Frank, 1986) and can keep small males from maintaining territories (e.g. as in collared lizards, Crotaphytus collaris, Baird & Timanus, 1998). Stress and inhibition can also increase the levels of stress hormones in the much smaller females, making it difficult for females to court, mate and lay their eggs successfully (Pottinger, 1999).
Although both effects tend to reduce the overall number of iguanas in the population, they may persist even in very dense populations if anthropogenic usage also helps to recruit animals from neighbouring areas. Studies of the rate of turnover in particularly dense populations are clearly needed to explore this issue more directly.
The social organization in the high anthropogenic usage sites is also notably different from that in low anthropogenic usage sites, in that a greater number of males are interacting with no females. In low anthropogenic usage sites, each male regularly interacts with one female. In high anthropogenic usage sites more than 40% of males did not interact with any females. Access to females is required for mating, so this result suggests that many more males in the high anthropogenic usage sites are not mating.
Dominant males in high anthropogenic usage sites may have more access to females and consequently sire more offspring, increasing the reproductive variance of males in these sites. If fewer males are responsible for offspring paternity, population viability may be reduced through inbreeding or the accumulation of deleterious alleles through genetic drift in a small population (Lande & Barrowclough, 1987). This result points to the importance of linking behaviour and the demographic consequences of that behaviour for the conservation of endangered animals. A behavioural shift of the sort observed in this study could have profound effects on the genetic health and long-term survival of iguana populations.
Cyclura iguanas are behaviourally complex, and among species and populations there are considerable differences in Cyclura displays (Martins & Lamont, 1998; Bissell & Martins, in press). Other species have also evolved unique functions for the head bob display (Martins & Lacy, in press). With such rapid change in behaviour, considerations for future conservation efforts for any Cyclura species must consider possible behavioural isolation of populations exposed to different levels of human habitat usage. Of course, if human influence is removed from an area, the once influenced populations may revert somewhat quickly to normal behavioural patterns. This study also demonstrates that detailed examination of a species in a portion of their habitat that has already been compromised or destroyed may not yield the most accurate results for demographic model predictions, especially if their social organization has changed. Therefore, careful consideration must be made when choosing populations on which to base demographic data for viability analysis. It is also important to consider behavioural ecology in the design and implementation of recovery, reintroduction and relocation programmes. The potential for behavioural changes needs to be considered for head starting and reintroduction plans because of the chances of aberrant behaviour developing (Dodd & Seigel, 1991).

Birds of Asia and Africa



Birds of Asia

Asia, the largest of the world's continents, has a wide variety of climates. These include tropical rain forests, temperate forests, deserts, marshlands, and Arctic tundra. Such birds as broadbills, fairy-bluebirds, fruit-doves, hornbills, and leafbirds inhabit Asian forests. The male rhinoceros hornbill, like other tree-nesting hornbills, walls up his mate into a nest hole while she incubates the eggs. The golden-fronted leafbird lives in monsoon forests, which have a long dry season followed by a season of heavy rainfall. The trees in a monsoon forest usually shed their leaves during the dry season and leaf out again at the start of the rainy season. The golden-fronted leafbird feeds on fruit and insects. The blue-backed fairy-bluebird and the lesser green broadbill eat mainly fruit. Many tropical southeast Asian birds, such as the blue-winged pitta and purple-throated sunbird, have multicolored plumage.



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The Himalaya, the great mountain range in southern Asia, is a biologically rich area with many species of birds. The foothills of the Himalaya provide a home to several brightly colored members of the pheasant family, including the Himalayan monal and Lady Amherst's pheasant. The Himalayan monal lives in forests above 10,000 feet (3,000 meters) high. The male has a loud ringing call. The common myna inhabits dry hillsides in India.

Some cultivated areas of Asia have become habitats for such species as the coppersmith barbet and the Java sparrow. The coppersmith barbet lives in open woodland, including orchards and gardens. It has a distinctive, monotonous "tonk" call, which it repeats over long periods. The Java sparrow was originally native to the islands of Bali and Java but has been widely introduced to other regions. It commonly resides in open areas, including rice fields, and has become a popular pet.


Birds of Africa

The Sahara, a vast desert, stretches across northern Africa and separates the continent's northern Mediterranean coastline from the land to the south. As a result, Mediterranean Africa shares many bird species with southern Europe. South of the Sahara, much of Africa has a tropical climate and a richer bird life. Rain forests provide homes for such colorful birds as the emerald cuckoo, yellow-bellied wattle-eye, and hammerkop. Many kinds of weavers live in open woodlands. The tropical grasslands have two of the world's tallest birds, the ostrich and the secretary-bird, as well as guineafowl and the crowned crane. Water birds of tropical Africa include the shoebill, the African fish-eagle, and various ducks, jacanas, kingfishers, and pelicans. Madagascar, a large island off the southeast African coast, has many unique birds, including the cuckoo roller and the helmet vanga.

Birds of the Seacoasts and Arctic

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Birds of the seacoasts

Some American and Canadian water birds normally nest along seacoasts. Along the Atlantic coast, such birds include the American oystercatcher, black skimmer, and common tern. The black oystercatcher, western gull, and Cassin's auklet nest along the Pacific coast. The brown pelican, laughing gull, and Wilson's plover nest along both coasts. Some species, such as oystercatchers and plovers, are shore birds. Certain others, including auks and auklets, gulls, and terns, sometimes hunt fish far out at sea.

In winter, the southeast, south, and southwest coasts of North America provide homes to numerous ducks, geese, and many other birds that nest in the Arctic. Many sandpipers and other Arctic birds visit U.S. and Canadian shores en route to winter homes in the tropics.


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Birds of the Arctic

Northernmost North America, Asia, and Europe lie in the Arctic. Most of this land is tundra-that is, cold, dry, treeless marshland. The Arctic tundra remains frozen solid most of the year. It comes to life briefly in spring and summer. At that time, the tundra provides a rich source of the insects and other small animals that birds eat. Many birds that winter in warmer climates arrive in the tundra to breed. Most are water birds. They include the lesser golden-plover, Arctic tern, Canada goose, parasitic jaeger, red phalarope, and many species of ducks and sandpipers. Land birds that migrate to the tundra include the horned lark and snow bunting.

Only a few birds live in the Arctic all year. Probably the best known are ptarmigans. These extremely hardy, chickenlike birds survive almost entirely on twigs and leaf buds during the long Arctic winters.

Birds of inland waters and marshes

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Most water birds swim after their food or dive or wade into the water for it. Few water birds live near fast-moving rivers because swimming, diving, and wading are difficult in a strong current. Lakes, ponds, and marshes are the chief freshwater habitats of birds. The birds nest on the shores of lakes and ponds and on high ground in marshes.

Typical swimming and diving birds of U.S. and Canadian fresh waters include the American coot, California gull, common loon, horned grebe, king rail, and many kinds of ducks. Among the ducks are the American wigeon, blue-winged teal, canvasback, and shoveler. Although some of these birds are excellent swimmers, a number of them feed mostly by wading at the edge of the water. Common wading birds include the American bittern, common snipe, great blue heron, and spotted sandpiper.

Some land birds have adopted ways of life that keep them near water. For example, the marsh wren, common yellowthroat, and red-winged blackbird often nest in marshes. The Louisiana waterthrush nests on the banks of streams and feeds on water insects. Belted kingfishers perch alongside bodies of water. Kingfishers dive after fish that swim near the surface and catch them with their bills.

Some birds of inland waters and marshes also live in saltwater environments. For example, the belted kingfisher, great blue heron, and green-backed heron often nest near the ocean and hunt fish in the shallow coastal waters. Most water birds of the United States and Canada fly south for the winter. Many of these birds make their winter homes near salt water.

Birds of brushy areas and the desert

Birds of brushy areas

Some birds make their home in and around brushy areas, which are covered by bushes and low scrubby trees. Such areas commonly occur on the edges of forests and woodlands, between woodlands and grasslands, and in abandoned fields that are developing into woodlands. Brushy areas exist throughout the United States and southern Canada. Many of the birds that live in these habitats are also wide ranging. They include the eastern towhee, gray catbird, loggerhead shrike, rufous-sided towhee, and yellow-breasted chat. Other birds of brushy habitats have a more limited range. The bobwhite and Carolina wren are permanent residents in the southeastern United States and in Mexico. The painted bunting nests chiefly in the southeastern half of the United States but migrates to Mexico in winter.


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Birds of the desert

Many birds that live in the deserts of the southwestern United States nest in saguaros and other large cactuses. The cactus wren builds its nest among cactus spines. Gila woodpeckers and gilded flickers nest in holes that they make in cactus stems. Elf owls, the smallest owls in the world, nest in holes that the woodpeckers abandon. A large percentage of desert birds chiefly eat animal flesh or insects. The deserts are dry, and such a diet provides more moisture than a diet of seeds. Meat-eating birds, including the golden eagle, roadrunner, and various species of owls, rank among the most common desert birds. Most of the cactus dwellers mainly eat insects. Gambel's quail and several species of sparrows are among the few ground-nesting, seed- eating birds of the North American deserts.

Birds of grasslands

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Until the mid-1800's, prairies covered much of central North America. The tall prairie grasses were a favorite nesting place of many birds. Today, most prairies have been plowed under for use as cropland. The birds that have adjusted best to these changes are those that traditionally nest in other open areas in addition to prairies. Such birds include the American kestrel, dickcissel, horned lark, vesper sparrow, western kingbird, and western meadowlark. Today, these birds nest as readily in or near hayfields and other cultivated grasslands as they do in native prairies. Horned larks even nest on golf courses.

Some prairie birds have had great difficulty adjusting to the changes in their habitat. For example, prairie-chickens once ranked among the most numerous prairie birds. But prairie-chickens nest only among tall grasses. Today, they live only in the few remaining native prairies.

Dry grasslands, now used mostly for grazing cattle, cover much of the western parts of the United States and Canada. Birds that nest in these grasslands include the burrowing owl, lark bunting, scissor-tailed flycatcher, and Baird's sparrow. Except for the burrowing owl, these birds have fared better than many of the prairie birds because their nesting places have been less disturbed by agriculture. Burrowing owls traditionally nest in prairie dog burrows. Ranchers have regarded prairie dogs as pests, however, and have tried to destroy their burrows. In so doing, they have wiped out the nesting places of the owls.

Birds of forests and woodlands

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Some North American birds live chiefly in needleleaf forests-that is, forests in which the dominant trees have narrow, needlelike leaves, such as firs, pines, and spruces. Needleleaf forests cover much of Canada and Alaska and mountainous areas of the western United States. Typical birds of these forests include the Blackburnian warbler, common creeper, gray jay, red-breasted nuthatch, ruby-crowned kinglet, and winter wren.

Certain other birds live chiefly in forests of broadleaf trees, which have broad, flat leaves that fall off each autumn. Such trees include the ash, beech, elm, maple, and oak. Broadleaf forests grow mainly in the eastern half of the United States and southeastern Canada. Typical birds of these forests include the American redstart, Baltimore oriole, ovenbird, scarlet tanager, tufted titmouse, and white-breasted nuthatch. Some birds, such as the hairy woodpecker and yellow-bellied sapsucker, inhabit both needleleaf forests and broadleaf forests.

Certain birds prefer open woodlands to dense forests. Open woodlands are areas of scattered trees. They are found mainly on the edges of forests, along riverbanks, and in suburban areas. Birds that nest in open woodlands include the cedar waxwing, downy woodpecker, house wren, rosebreasted grosbeak, yellow-billed cuckoo, and northern flicker. Red-eyed vireos live in almost any area that has broadleaf trees.

Many birds inhabit a particular level of a forest or woodland. For example, grosbeaks, tanagers, and many kinds of wood warblers live mainly in the treetops. Nuthatches and woodpeckers live farther down on the branches and trunks. Ovenbirds and winter wrens live chiefly on the forest or woodland floor.

Birds of North America

More than 700 species of birds live in North America north of Mexico, a region that includes all of Canada and all of the United States except Hawaii. Most of this region lies in the northern temperate zone. In the southern part of the region, many of the birds are permanent residents. In the northern part, most of the birds are summer residents only. In summer, the birds mate, lay and hatch their eggs, and raise their families. They then fly south for the winter. Mexico and Central America are part of North America. But most of the birds that reside there permanently are more closely related to those of South America than to U.S. and Canadian birds.

The birds of temperate North America live in seven main kinds of habitats: (1) urban areas, (2) forests and woodlands, (3) grasslands, (4) brushy areas, (5) deserts, (6) inland waters and marshes, and (7) seacoasts. Some North American birds live north of the temperate zone-that is, in the Arctic.





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Birds of urban areas

Many birds will nest in urban areas if these areas have nesting places similar to those of the birds' natural habitat. In addition to pigeons and starlings, such birds include robins, blue jays, mockingbirds, cardinals, wrens, common crows, grackles, and house sparrows. Cardinals and mockingbirds usually nest in shrubs or low trees. Robins and blue jays nest in shade trees. Wrens nest inside tree holes, bird boxes, and even mailboxes. House sparrows and pigeons, both introduced from Europe, rank among the most common birds in North American cities. They will nest in almost any small opening. Such birds remain a familiar sight even in the downtown areas of big cities.
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