Climate change and size evolution in an island rodent species: new perspectives on the island rule

As stated by the island rule, small mammals evolve toward gigantism on islands. In addition they are known to evolve faster than their mainland counterparts. Body size in island mammals may also be influenced by geographical climatic gradients or climatic change through time. We tested the relative effects of climate change and isolation on the size of the Japanese rodent Apodemus speciosus and calculated evolutionary rates of body size change since the last glacial maximum (LGM). Currently A. speciosus populations conform both to Bergmann's rule, with an increase in body size with latitude, and to the island rule, with larger body sizes on small islands. We also found that fossil representatives of A. speciosus are larger than their extant relatives. Our estimated evolutionary rates since the LGM show that body size evolution on the smaller islands has been less than half as rapid as on Honshu, the mainland-type large island of Japan. We conclude that island populations exhibit larger body sizes today not because they have evolved toward gigantism, but because their evolution toward a smaller size, due to climate warming since the LGM, has been decelerated by the island effect. These combined results suggest that evolution in Quaternary island small mammals may not have been as fast as expected by the island effect because of the counteracting effect of climate change during this period.     

Home range and mating system of two sympatric field mouse species,Apodemus speciosus andApodemus argenteus

The size and spatial distribution of home ranges in two sympatric field mouse species,Apodemus speciosus andApodemus argenteus, were revealed by the capture-recapture method in a temperate deciduous forest from June 1987 to June 1990. InA. speciosus, the home ranges of males were significantly larger tha those of females, and overlapped with those of other males and females during the breeding season. InA. argenteus, the home range of each male overlapped only that of a single female throughout the year. These results suggested thatA. speciosus was promiscuous or polygynous andA. argenteus was monogamous.     

Rule reversal: Ecogeographical patterns of body size variation in the common treeshrew (Mammalia,Scandentia)

There are a number of ecogeographical “rules” that describe patterns of geographical variation among organisms. The island rule predicts that populations of larger mammals on islands evolve smaller mean body size than their mainland counterparts, whereas smaller‐bodied mammals evolve larger size. Bergmann's rule predicts that populations of a species in colder climates (generally at higher latitudes) have larger mean body sizes than conspecifics in warmer climates (at lower latitudes). These two rules are rarely tested together and neither has been rigorously tested in treeshrews, a clade of small‐bodied mammals in their own order (Scandentia) broadly distributed in mainland Southeast Asia and on islands throughout much of the Sunda Shelf. The common treeshrew, Tupaia glis, is an excellent candidate for study and was used to test these two rules simultaneously for the first time in treeshrews. This species is distributed on the Malay Peninsula and several offshore islands east, west, and south of the mainland. Using craniodental dimensions as a proxy for body size, we investigated how island size, distance from the mainland, and maximum sea depth between the mainland and the islands relate to body size of 13 insular T. glis populations while also controlling for latitude and correlation among variables. We found a strong negative effect of latitude on body size in the common treeshrew, indicating the inverse of Bergmann's rule. We did not detect any overall difference in body size between the island and mainland populations. However, there was an effect of island area and maximum sea depth on body size among island populations. Although there is a strong latitudinal effect on body size, neither Bergmann's rule nor the island rule applies to the common treeshrew. The results of our analyses demonstrate the necessity of assessing multiple variables simultaneously in studies of ecogeographical rules.     

Competition, coexistence, and adaptation amongst rodent invaders to Pacific and New Zealand islands

Variation in skull size was investigated for three species of rats (kiore –Rattus exulans Peale; ship rat –R. rattus L.; Norway rat –R. norvegicus Berkenhout) which were introduced by humans to various islands in New Zealand and other Pacific islands. Data from seventy-one islands and 882 specimens are examined for evidence of the effects of latitude, island size and interspecific competition among rats and the house mouse (Mus musculus L.) on skull size, using multiple regressions. For R. exulans, skull size increases with latitude as predicted by Bergmann's rule, but no such effect occurs for the other two rats. There was a positive relationship between island size and the number of species inhabiting it, and some species combinations were more likely to occur than others. For example, R. exulans and R. norvegicus were more likely to occur together, while R. rattus and R. exulans were rarely sympatric. R. exulans and R. rattus skull size was negatively correlated with the number of other rodents on the same island. R. exulans skull size increased on smaller islands in some island groups, perhaps because increased density and consequent increased intraspecific competition on smaller islands favours increased body size. This effect is more pronounced in tropical islands (Solomon islands), than in subtropical ones (Hawaiian islands) and less so in temperate New Zealand. Collectively the data demonstrate that rapid evolution of body size in predictable directions can follow within 150 years of the introduction of species to new receiving communities.     

Evolutionary and biogeographical implications of variation in skull morphology of raccoon dogs (Nyctereutes procyonoides,Mammalia: Carnivora)

Morphological characteristics reflect geographical variation resulting from adaptation to varying environmental conditions. Carnivore species distributed over a wide geographical range generally have highly polymorphic morphological variation. The raccoon dog (Nyctereutes procyonoides) has a longitudinal distribution restricted to East Asia and the northern Indochina Peninsula. Its unique geographical range makes it an appropriate model to examine how morphological differences are influenced by geography. To demonstrate morphological evolution of Russian, Chinese, Korean and Japanese raccoon dogs predicted by geographical differences, we tested the island rule and Bergmann's rule. We compared craniodental variation among populations and examined morphological implications for intraspecific taxonomic status. Insular raccoon dogs possessed substantially smaller body size than those from the mainland. Moreover, different island effects among Japanese islands were demonstrated by markedly larger occipital condyle breath in the Hokkaido population. Larger skull size in Russian and Hokkaido raccoon dogs could be explained by Bergmann's rule. Based on previous chromosomal and molecular studies and results of our morphological analyses, we suggest Japanese raccoon dogs are a distinct species from the mainland N. procyonoides.     

Utilization of different prey type patches in the Ural owl(Strix uralensis): a sit-and-wait predator

To quantify the pattern of allocation of foraging activity ofa sit-and-wait forager among feeding sites of different profitability,I conducted an experimental study of patch utilization behaviorof Ural owls (Strix uralensis) in an experimental flight cage.The owls were allowed to search among four patches containingequal numbers of mice, two with the large Japanese field mouse(Apodemus speciosus) and two with the small Japanese field mouse(A. argenteus). Patches with A. speciosus were more profitablethan those with A. argenteus, and owls visited more profitablepatches more frequently. Visiting frequency to richer patchesdid not increase with experience; however, owls changed searchtime according to experience. Search time in a patch becamelonger in later visits than in earlier visits during a givennight according to an owl’s sampling experience amongpatches. Furthermore, owls stayed longer in richer patches thanin poor ones if they had caught mice in both types of patches.Search time had great variance. Mean search time that endedwith attack was longer than that ended without attack (giveup). In effect, Ural owls improved their resource utilizationpattern as they accumulated experience in the environment. [BehavEcol 1991;2:99–105J]     

Geographic variation in walnut seed size correlates with hoarding behaviour of two rodent species

Seeds of the Japanese walnut, Juglans ailanthifolia, are usually scatter-hoarded by two rodent species, the Japanese squirrel Sciurus lis and the field mouse Apodemus speciosus, but only by the latter in several areas where S. lis is absent. We examined seed-size-mediated interactions of these three species across a wide geographic range. Field tracking of walnuts with miniature radio-transmitters revealed that squirrels hoarded larger seeds more frequently and at greater distances than smaller seeds. In contrast, mice hoarded smaller seeds more frequently and transported them farther than larger seeds. These seed dispersers could affect the evolution of seed size because seeds hoarded at sites farther from source trees are known to survive better until germination and as seedlings. We expect that larger seeds may be advantageous in regeneration if the main seed dispersers are squirrels, whereas smaller seeds may be advantageous if mice are the dominant dispersers. These predictions were supported by the fact that seed size was smaller on islands inhabited only by mice and at the edge of the squirrel distribution, compared to areas where mice and squirrels are both common.     

A Biogeographic View of Apodemus in Asia and Europe Inferred From Nuclear and Mitochondrial Gene Sequences

Sequences of the mitochondrial cyt b gene and nuclear IRBP, RAGI, I7, and vWF genes were used to assess the evolutionary history of major lineages of Apodemus, in particular to better understand dispersal between Asia and Europe. Our data show eight extant lineages of Late Tertiary origin: Apodemus agrarius, A. semotus, A. peninsulae, A. speciosus, A. argenteus, A. gurkha, A. mystacinus, and A. sylvaticus. Monophyly of two European lineages (A. mystacinus and A. sylvaticus) and four Asian lineages (A. agrarius, A. semotus, A. peninsulae, and A. speciosus) was confirmed with high bootstrap support. Together with literature data, the available molecular data depict three crucial evolutionary events: (1) initial wide dispersal and subsequent radiation around 6 million years ago, (2) region-specific radiations in Europe and southern China around 2 million years ago, and (3) westward dispersal of A. agrarius to Europe in the Late Quaternary.     

Role of interspecific competition in the coexistence ofApodemus argenteus andA. speciosus (Rodentia: Muridae)

Reciprocal-removal experiments with two replicates were conducted to test for the role of interspecific competition in the coexistence ofApodemus argenteus andA. speciosus. Population density, rate of appearance of new (unmarked) individuals, reproduction, survival rate and habitat use were monitored during pre- and removal periods. In both removal experiments, the removal ofA. argenteus had little effect onA. speciosus, while that ofA. speciosus affected several population characteristics ofA. argenteus. Namely, the removal ofA. speciosus shifted the distribution ofA. argenteus to the habitat with a denser shrub cover in one experiment. Also, the removal increased the population densities and appearance rates of new individuals ofA. argenteus in another experiment. Interspecific interactions between the two species appeared to be a one-way action fromA. speciosus toA. argenteus. In removal periods in both experiments, the rates of appearance of new individuals in each species were the highest on the grid where that species was removed. These results suggest that, though interspecific competition occurred between the two species, intraspecific competition had greater effects than interspecific competition on the abundance and habitat use ofA. argenteus andA. speciosus. This implies that the fundamental niches ofA. argenteus andA. speciosus differ potentially, which may play an important role in the coexistence of the two species.     

Hoarding behaviors of two wood mouse species: Different preference for acorns of two Fagaceae species

Two species of wood mouse, Apodemus argenteus and A. speciosus, were observed consuming and hoarding acorns of Quercus serrata and Castanopsis cuspidata. When each species of acorn was supplied individually, both species of mice used each species of acorn for eating and hoarding. When both species of acorn were supplied, A. argenteus consumed or hoarded only C. cuspidata, whereas A. speciosus tended to eat C. cuspidata acorns at the feeding site, and disperse or hoard Q. serrata acorns. Apodemus speciosus is unlikely to disperse C. cuspidata acorns (their utilization was biased towards consumption) when Q. serrata acorns are also available. Apodemus argenteus will make almost no contribution to the dispersal of Q. serrata when the two acorn species coexist.     

A note on the presence of B chromosome in the small Japanese field mouse,Apodemus argenteus,in central Honshu,Japan

Previously, many studies have revealed the presence of B chromosomes in wild mouse taxa of the genus Apodemus (Rodentia, Muridae). In one of the Apodemus species, A. argenteus, which is endemic to Japan, it is known that B chromosomes were confirmed only in individuals (2n = 46 + B chromosome) from Hokkaido, Japan. There is no report of the presence of B chromosomes from other localities in the Japanese Islands. In this study, we analyzed the chromosomal constitutions of 43 individuals of A. argenteus from three localities in Honshu, Japan. A total of three individuals from central Honshu showed 2n = 47, and each individual carried a dot-like B chromosome. In addition, these B chromosome features were analyzed by differential staining methods, and the C- and QM-banding patterns of the B chromosomes were identical to those of the X chromosomal heterochromatic region showing the delayed-fluorescent response. Thus, it is considered that these B chromosomes would be derived from the heterochromatin of the X chromosomes, as reported in previously published papers.     

Evolution of restriction sites of ribosomal DNA in natural populations of the field mouse,Apodemus speciosus

An analysis by restriction endonuclease digestion of ribosomal DNA (rDNA) was carried out in natural populations of Apodemus speciosus, a field mouse that is endemic to Japan. Two restriction sites, the EcoRI (E3) and DraI (D4) sites, in the nontranscribed spacer region downstream from the gene for 28S RNA showed polymorphism within and between individuals in the populations from the Japanese main islands. By contrast, populations from the small adjoining islands which are thought to have separated from the main islands 1–2 × 10⁴ years ago showed relatively low levels of polymorphism within and between individuals, i.e., one of the polymorphic bands in the case of each enzyme was predominant in these populations, irrespective of the variants. These results indicate that the rate of fixation of site variations depends on population size and that the direction of fixation is random. Furthermore, each polymorphic restriction site seems to be fixed independently.Correspondence to: H. Suzuki     

Evolutionary size changes in plants of the south‐west Pacific

Aim To investigate evolutionary changes in the size of leaves, stems and seeds of plants inhabiting isolated islands surrounding New Zealand. Location Antipodes, Auckland, Campbell, Chatham, Kermadec, Three Kings and Poor Knights Islands. Methods First, we compared the size of leaves and stems produced by 14 pairs of plant taxa between offshore islands and the New Zealand mainland, which were grown in a common garden to control for environmental effects. Similar comparisons of seed sizes were made between eight additional pairs of taxa. Second, we used herbarium specimens from 13 species pairs to investigate scaling relationships between leaf and stem sizes in an attempt to pinpoint which trait might be under selection. Third, we used herbarium specimens from 20 species to test whether changes in leaf size vary among islands located at different latitudes. Lastly, we compiled published records of plant heights to test whether insular species in the genus Hebe differed in size from their respective subgenera on the mainland. Results Although some evidence of dwarfism was observed, most insular taxa were larger than their mainland relatives. Leaf sizes scaled positively with stem diameters, with island taxa consistently producing larger leaves for any given stem size than mainland species. Leaf sizes also increased similarly among islands located at different latitudes. Size changes in insular Hebe species were unrelated to the average size of the respective subgenera on the mainland. Main conclusions Consistent evidence of gigantism was observed, suggesting that plants do not obey the island rule. Because our analyses were restricted to woody plants, results are also inconsistent with the ‘weeds‐to‐trees’ hypothesis. Disproportionate increases in leaf size relative to other plant traits suggest that selection may favour the evolution of larger leaves on islands, perhaps due to release from predation or increased intra‐specific competition.     

The fiddler crab,Minuca pugnax,follows Bergmann's rule

Bergmann's rule predicts that organisms at higher latitudes are larger than ones at lower latitudes. Here, we examine the body size pattern of the Atlantic marsh fiddler crab, Minuca pugnax (formerly Uca pugnax), from salt marshes on the east coast of the United States across 12 degrees of latitude. We found that M. pugnax followed Bergmann's rule and that, on average, crab carapace width increased by 0.5 mm per degree of latitude. Minuca pugnax body size also followed the temperature–size rule with body size inversely related to mean water temperature. Because an organism's size influences its impact on an ecosystem, and M. pugnax is an ecosystem engineer that affects marsh functioning, the larger crabs at higher latitudes may have greater per‐capita impacts on salt marshes than the smaller crabs at lower latitudes.     

Area, isolation and body size evolution in insular carnivores

Body sizes of insular mammals often differ strikingly from those of their mainland conspecifics. Small islands have reduced numbers of competitor and predator species, and more limited resources. Such reductions are believed to select for predictable changes in body sizes, with large mammals growing progressively smaller as island area decreases, while small ones grow progressively larger. Medium-sized mammals are thought to be largest on intermediate-sized islands. Increased isolation is seen as promoting insular gigantism. We searched for such patterns using a large database of insular carnivore specimens. Neither small nor large carnivores show a consistent area/body size relationship. Medium-sized carnivores are no more likely to attain large size on medium-sized islands then they are to be small there. We found no consistent patterns of body size variation in relation to isolation.     

Stranded on an island: consequences of forest fragmentation for body size variations in an arboreal mammal, the edible dormouse (Glis glis)

The island rule states that small mammals isolated on islands have the evolutionary tendency to become larger, while large mammals tend to become smaller. However, the underlying mechanisms and life history consequences of these insular shifts in body size still remain speculative. The aim of this study was to investigate whether an arboreal mammal, the edible dormouse (Glis glis), showed shifts in body size when inhabiting isolated forest fragments. We analysed a data set of 541 individuals captured between 2005 and 2010 in four different forest fragments and one continuous forest, which served as a reference area. Sex, age, body mass, and size of all individuals were known. We used linear mixed-effect models to investigate whether individuals differed in their body size and mass between forest fragments and continuous forest. Our study revealed that edible dormice inhabiting forest fragments were significantly larger and heavier than individuals in the continuous forest, in accordance with patterns described by the island rule for small mammals. Because edible dormice frequently use nest boxes to rest during the day and to rear offspring, the life history strategies of this rodent can be easily investigated under evolutionary relevant conditions in the field. Thus the edible dormouse represents an excellent model organism for studying the mechanisms underlying shifts in body size as a response to habitat fragmentation and to investigate the consequences of these shifts on their life history strategies.     

Parasites and the island syndrome: the colonization of the western Mediterranean islands by Heligmosomoides polygyrus (Dujardin, 1845)

Aim Populations of free‐living vertebrates on islands frequently differ from their mainland counterparts by a series of changes in morphometric, life‐history, behavioural, physiological and genetic traits, collectively referred to as the ‘island syndrome’. It is not known, however, whether the ‘island syndrome’ also affects parasitic organisms. The present study establishes the colonization pattern of the Mediterranean islands by the nematode Heligmosomoides polygyrus, a direct and specific parasite of rodent hosts of the Apodemus genus, and evaluates the effects of island colonization by this species on two components of the island syndrome: the loss of genetic diversity and the enlargement of the ecological niche. Location Heligmosomoides polygyrus was sampled on seven western Mediterranean islands ? Corsica, Crete, Elba, Majorca, Minorca, Sardinia and Sicily ? as well as in 20 continental locations covering the Mediterranean basin. Methods The mitochondrial cytochrome b gene (690 base pairs) was sequenced in 166 adult H. polygyrus individuals sampled in the 27 continental and island locations. Phylogenetic reconstructions in distance, parsimony, maximum likelihood and Bayesian posterior probabilities were carried out on the whole cytochrome b gene data set. The levels of nucleotide, haplotype and genetic divergence (Kimura two‐parameter distance estimator) diversities were estimated in each island population and in the various continental lineages. Results Phylogenetic reconstructions show that the mainland origins of H. polygyrus were continental Spain for the Balearic Islands (Majorca, Minorca), northern Italy for the Tyrrhenian Islands (Corsica, Sardinia, Elba), southern Italy for Sicily, and the Balkan region for Crete. A comparison of island H. polygyrus populations with their mainland source populations revealed two characteristic components of the island syndrome in this parasite. First, island H. polygyrus populations display a significant loss of genetic diversity, which is related (r² = 0.73) to the distance separating the island from the mainland source region. Second, H. polygyrus exhibits a niche enlargement following insularization. Indeed, H. polygyrus in Corsica is present in both A. sylvaticus and Mus musculus domesticus, while mainland H. polygyrus populations are present exclusively in Apodemus hosts. Main conclusions Our results show that H. polygyrus has undergone a loss of genetic diversity and a niche (host) enlargement following colonization of the western Mediterranean islands. To our knowledge, this study provides the first evidence for components of the ‘island syndrome’ in a parasitic nematode species.     

Hoarding of acorns by granivorous mice and its role in the population processes of Pasania edulis (Makino) Makino

In order to evaluate the role of granivorous mice, Apodemus speciosus Temminck and Apodemus argenteus Temminck, in the regeneration of Pasania edulis (Makino) Makino, an evergreen tree, we conducted field studies examining acorn crops, the population dynamics and hoarding behavior of mice and pre- and postdispersal acorn predation in an evergreen broad-leaved forest dominated by P.edulis in Kagoshima, southern Japan. The study was conducted from 1994 to 2000. Apodemus mice selected sound acorns and hoarded them in the soil after transporting them for distances ranging from 5.4 to 19.9m. This behavior appeared to be beneficial to the establishment of seedlings of P.edulis. However, the positive effects were negated by a high rate of recovery of the acorns hoarded by the mice. A life-table analysis of five cohorts of P.edulis indicated that postdispersal predation of acorns by Apodemus mice was a major contributor to annual variation in the number of new seedlings. A considerable number of acorns germinated only in years with a good acorn crop and a low level of resident mice. These results suggest that Apodemus mice are serious acorn predators rather than important dispersers. After germination, acorns were attacked by the acorn borer at a high rate. From these results, we can conclude that acorn production probably makes a smaller contribution to the regeneration of P.edulis than coppice shoot production at the study site.     

‘On being the right size’ – Do aliens follow the rules?

Aim

To assess whether mammalian species introduced onto islands across the globe have evolved to exhibit body size patterns consistent with the ‘island rule,’, and to test an ecological explanation for body size evolution of insular mammals.

Location

Islands worldwide.

Methods

We assembled data on body mass, geographical characteristics (latitude, maximum elevation) and ecological communities (number of mammalian competitors, predators and prey) for 385 introduced populations across 285 islands, comprising 56 species of extant, non‐volant mammals. We used linear regression, ANCOVA and regression tree analyses to test whether introduced populations of mammals exhibit the island rule pattern, whether the degree of body size change increased with time in isolation and whether residual variation about the general trend can be attributed to the geographical and ecological characteristics of the islands.

Results

Introduced populations follow the predicted island rule trend, with body size shifts more pronounced for populations with greater residence times on the islands. Small mammals evolved to larger body sizes in lower latitudes and on islands with limited topographic relief. Consistent with our hypothesis on the ecology of evolution, body size of insular introduced populations was influenced by co‐occurring species of mammalian competitors, predators and prey.

Conclusion

The island rule is a pervasive pattern, exhibited across a broad span of geographical regions, taxa, time periods and, as evidenced here, for introduced as well as native mammals. Time in isolation impacts body size evolution profoundly. Body size shift of introduced mammals was much more pronounced with increasing residence times, yet far less than that exhibited by native, palaeo‐insular mammals (residence times > 10,000 years). Given the antiquity of many species introductions, it appears that much of what we view as the natural character and ecological dynamics of recent insular communities may have been rendered artefacts of ancient colonizations by humans and commensals.