Theunis Piersma

The interplay between habitat availability and population differentiation

We present STRUCTURE HARVESTER (available at http://taylor0.biology.ucla.edu/structureHarvester/), a web-based program for collating results generated by the program STRUCTURE. The program provides a fast way to assess and visualize likelihood values across multiple values of K and hundreds of iterations for easier detection of the number of genetic groups that best fit the data. In addition, STRUCTURE HARVESTER will reformat data for use in downstream programs, such as CLUMPP.

Phenotypic flexibility and the evolution of organismal design

Evolutionary biologists often use phenotypic differences between species and between individuals to gain an understanding of organismal design. The focus of much recent attention has been on developmental plasticity - the environmentally induced variability during development within a single genotype. The phenotypic variation expressed by single reproductively mature organisms throughout their life, traditionally the subject of many physiological studies, has remained under-exploited in evolutionary biology. Phenotypic flexibility, the reversible within-individual variation, is a function of environmental conditions varying predictably (e.g. with season), or of more stochastic fluctuations in the environment. Here, we provide a common framework to bring the different categories of phenotypic plasticity together, and emphasize perspectives on adaptation that reversible types of plasticity might provide. We argue that better recognition and use of the various levels of phenotypic variation will increase the scope for phenotypic experimentation, comparison and integration.

Rapid reversible changes in organ size as a component of adaptive behaviour

Organ structures and correlated metabolic features (e.g. metabolic rate) have often taken as fixed attributes of fully grown individual vertebrates. When measurements of these attributes became available they were often used as representative values for the species, disregarding the specific conditions during which the mesurement were made. Evidence is accumulating that the functional size of organs and aspects of the metabolic physiology of an individual may show great flexibility over timescales of weeks and even days depending on physiological status, environmental conditions and behavioural goals. This flexibility is a way for animals to cope successfully with a much wider range of conditions occurring during various life-cycle events than fixed metabolic machinery would allow. Such phenotypic flexibility is likely to be a common adaptive syndrome, typical of vertebrates living in variable environments.

Rapid population decline in red knots: fitness consequences of decreased refuelling rates and late arrival in Delaware Bay

Most populations of migrant shorebirds around the world are in serious decline, suggesting that vital condition–dependent rates such as fecundity and annual survival are being affected globally. A striking example is the red knot (Calidris canutus rufa) population wintering in Tierra del Fuego, which undertakes marathon 30 000 km hemispheric migrations annually. In spring, migrant birds forage voraciously on horseshoe crab eggs in Delaware Bay in the eastern USA before departing to breed in Arctic polar deserts. From 1997 to 2002 an increasing proportion of knots failed to reach threshold departure masses of 180–200 g, possibly because of later arrival in the Bay and food shortage from concurrent over–harvesting of crabs. Reduced nutrient storage, especially in late–arriving birds, possibly combined with reduced sizes of intestine and liver during refuelling, had severe fitness consequences for adult survival and recruitment of young in 2000–2002. From 1997 to 2002 known survivors in Delaware Bay were heavier at initial capture than birds never seen again, annual survival of adults decreased by 37% between May 2000 and May 2001, and the number of second–year birds in wintering flocks declined by 47%. Population size in Tierra del Fuego declined alarmingly from 51 000 to 27 000 in 2000–2002, seriously threatening the viability of this subspecies. Demographic modelling predicts imminent endangerment and an increased risk of extinction of the subspecies without urgent risk–averse management.

Extreme endurance flights by landbirds crossing the Pacific Ocean: ecological corridor rather than barrier?

Mountain ranges, deserts, ice fields and oceans generally act as barriers to the movement of land-dependent animals, often profoundly shaping migration routes. We used satellite telemetry to track the southward flights of bar-tailed godwits (Limosa lapponica baueri), shorebirds whose breeding and non-breeding areas are separated by the vast central Pacific Ocean. Seven females with surgically implanted transmitters flew non-stop 8117–11 680 km (10 153±1043 s.d.) directly across the Pacific Ocean; two males with external transmitters flew non-stop along the same corridor for 7008–7390 km. Flight duration ranged from 6.0 to 9.4 days (7.8±1.3 s.d.) for birds with implants and 5.0 to 6.6 days for birds with externally attached transmitters. These extraordinary non-stop flights establish new extremes for avian flight performance, have profound implications for understanding the physiological capabilities of vertebrates and how birds navigate, and challenge current physiological paradigms on topics such as sleep, dehydration and phenotypic flexibility. Predicted changes in climatic systems may affect survival rates if weather conditions at their departure hub or along the migration corridor should change. We propose that this transoceanic route may function as an ecological corridor rather than a barrier, providing a wind-assisted passage relatively free of pathogens and predators.

Rapid changes in the size of different functional organ and muscle groups during refueling in a long-distance migrating shorebird

The adaptive value of size changes in different organ and muscle groups was studied in red knots (Calidris canutus islandica) in relation to their migration. Birds were sampled on five occasions: at arrival in Iceland in May 1994, two times during subsequent refueling, at departure toward, and on return from, the high arctic breeding grounds. During their 24‐d stopover in May, body mass increased from 144.3 to 214.5 g. Mass gains were lowest over the first week (0.85 g/d, only fat‐free tissue deposited). Over the subsequent 10 d, average mass increased by 5.0 g/d (fat contributing 78%), and over the last week before takeoff, it increased by 2.0 g/d (fat contributing over 100% because of loss of lean components). There were no sex differences in body and fat mass gains. Over the first interval, lean masses of heart, stomach, and liver increased. During the middle 10 d, sizes of leg muscle, intestine, liver, and kidneys increased. Stomach mass decreased over the same interval. In the last interval before takeoff, the stomach atrophied further and the intestine, leg muscles, and liver became smaller too, but pectoral muscles and heart increased in size. Sizes of “exercise organs” such as pectoral muscle and heart were best correlated with body mass, whereas sizes of organs used during foraging (leg muscles) and nutrient extraction (intestine, liver) were best correlated with rate of mass gain. Kidneys changed little before takeoff, which suggests that they are needed as much during flight as during refueling.

Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure?

On the basis of associations between the characteristics of breeding and wintering habitats, apparent immunocompetence, and chick energetics of shorebirds (Charadrii), trade-offs between investments in immunofunctioning on the one hand and growth and sustained exercise on the other are suggested, that determine the year-round use of particular types of habitat by long-distance migrating shorebirds. Some species appear restricted to parasite-poor habitats (high arctic tundra, exposed seashores) where small investments in immunomachinery may suffice and even allow for high growth rates. However, such habitats are few and far between, necessitate long and demanding migratory flights in the course of an annual cycle and are often energetically costly to live in. Species evolutionarily opting for parasite-poor habitats may be rather susceptible to parasites and pathogens as a result of investments in sustained exercise (including thermoregulation) rather than immunocompetence. Components of this general hypothesis are perfectly testable, and such tests may shed new light on several other biogeographical, energetic and evolutionary riddles.

Empirical evidence for differential organ reductions during trans–oceanic bird flight

Since the early 1960s it has been held that migrating birds deposit and use only fat as fuel during migratory flight, with the non–fat portion of the body remaining homeostatic. Recent evidence from field studies has shown large changes in organ sizes in fuelling birds, and theory on fuel use suggests protein may be a necessary fuel during flight. However, an absence of information on the body condition of migrants before and after a long flight has hampered understanding of the dynamics of organs during sustained flight. We studied body condition in a medium–sized shorebird, the great knot (Calidris tenuirostris), before and after a flight of 5400 km from Australia to China during northward migration. Not only did these birds show the expected large reduction in fat content after migration, there was also a decrease in lean tissue mass, with significant decreases in seven organs. The reduction in functional components is reflected in a lowering of the basal metabolic rate by 46%. Recent flight models have tried to separate the ‘flexible’ part of the body from the constant portion. Our results suggest that apart from brains and lungs no organs are homeostatic during long–distance flight. Such organ reductions may be a crucial adaptation for long–distance flight in birds.

Interactions between stomach structure and diet choice in shorebirds

Captive Red Knots (Calidris canutus) fed soft food pellets developed atrophied stomachs, and were reluctant to eat their usual hard-shelled mollusc prey. An interspecific comparison among shorebirds showed that wild Red Knots and other intact-mollusc-eating species have gizzards with relatively great mass but very small proventriculi. Within six different shorebird species, the heavier individuals usually had the heavier stomachs as well, but in Red Knots and Bar-tailed Godwits (Limosa lapponica) we identified heavy premigrant individuals with reduced stomach masses, suggesting a reallocation of protein reserves before long-distance flights. In both species reduced stomach mass was associated with a relatively soft diet. We were unable to show that during adjustment of stomachs to hard-shelled prey, such prey are broken down to smaller fragments. We attribute this to the counteractive influence of the pylorus during adjustment. We summarize the suggested stomach/diet interactions as a network of causal relationships and feedback loops involving the type of diet and gizzard mass. We identify two basic modifiers of gizzard mass: one working via endurance training and disuse atrophy; and another involving endocrine and/or neural mechanisms. It is likely that, in the course of their annual cycle, shorebirds are prevented from achieving maximal digestive performance owing to seasonal changes in feeding habitats and diet enforced by their long-distance migrations.

Scale and intensity of intertidal habitat use by knots Calidris canutus in the Western Wadden Sea in relation to food, friends and foes

Abstract In August–October 1988–1992 we studied the distribution and abundance of knots Calidris canutus around Griend in the western Wadden Sea, and the extent to which these can be explained by benthic prey availability and presence of avian predators. Numbers in the nonbreeding season showed monthly averages of 10 000 to 25 000 birds. Over 100 000 knots were recorded on three occassions. Knots feed in large flocks, individual birds usually experiencing 4 000 to 15 000 flock-mates. The Siberian-breeding/west-African wintering canutus subspecies passed through in late July and early August. Otherwise the Greenlandic/Canadian breeding islandica subspecies was present. Over the period 1964–1992 there were no clear trends in the number of knots, but canutus -knots were particularly abundant in July–August 1991, whereas in 1992 both subspecies were absent. Macoma balthica was the preferred prey of both subspecies. Hydrobia ulvae, Mytilus edulis and Cerastoderma edule were eaten when Macoma was absent close to the surface of the sediment. As Macoma buried deeper from July onwards, canutus faced better average feeding conditions than islandica later in the year. The spatial distributon of knots feeding on the intertidal flats around Griend was best explained by the harvestable biomass of the prevalent prey species in a particular year and season, i.e. Macoma (main prey when their harvestable biomass densities were greater than ca 0.8 g AFDM per m 2 ) and Cerastoderma , and by the avoidance of situations where they run the risk of attack by bird-eating birds. Flocks of knots covered most of the intertidal flats in the Western Dutch Wadden Sea in a couple of tidal cycles. This is about 800 km 2 , much larger than the equivalent area used by knots on their wintering grounds in Mauritania (10–15 km 2 ), a difference that is correlated with prey spectrum, prey availability and predictability.