Published on
The New York Times

A World Out of Time

Leon Kreitzman

Spring is a busy season. Lambs are born in the spring, when there is plenty of fresh grass to sustain milk production in the mother and for the young to feed upon after weaning. The type of food that birds feed their young varies among species and determines breeding times. Rooks, for instance, breed early in the year because the earthworms they feed to their young move deeper into the soil as the warmer, drier days of spring and summer arrive. Finches feed seeds to their chicks, and so produce their young when the grasses have ripened.

But everything has to happen at the right time.

The winter moth caterpillar is partial to the leaves of apple and cherry trees, but any deciduous tree will do. Around Arnhem, in the Netherlands, it feeds on oak leaves. But the caterpillar has a delicate timing problem: it must hatch just when the new leaf buds burst open, revealing the young leaves. If it hatches too early, or too late, it may starve. Too early, and there are no leaves to eat; too late, and increased tannin concentrations make the leaves less digestible. Either circumstance leads to a lower weight at pupation or to a longer larval period, resulting in a higher probability of the caterpillar’s being eaten.

The date of the oak bud burst is cued largely by spring temperatures and can vary considerably from year to year. There is strong selection pressure on the winter moth to synchronize its egg hatching to the oak bud burst. But the moth’s timing mechanism is determined by the relationship between frost-days (below 0°C, or 32° F) and those days with a temperature above 3.9°C (39° F), rather than mean temperature alone.

And, over the past two decades, the pattern of the climate at Arnhem has been changing as well. Spring temperatures have risen and oak bud burst now occurs about 10 days earlier than it did 20 years ago. Caterpillars hatch 15 days earlier than before, overcompensating by five days for the change in the oaks. The caterpillars were already hatching several days before bud burst in 1985, so now they must wait on average about eight days for food, and they get very hungry.

Great tits (a common bird in Europe, a bit like a chickadee) in the Arnhem forests feed their young on the protein-rich winter moth caterpillars. The birds have eight or nine chicks in a brood, and each will eat about 70 caterpillars a day — that’s about 90 percent of their food intake. It takes about 18 days for the eggs of the great tit to incubate and hatch, so for them to make the most of the caterpillar splurge, timing is critical.

If the caterpillars emerge at precisely the right time, they can guzzle on the new oak leaves, and their population peaks just as the chicks need feeding. If the parent tits are a bit late, or — to put it another way — if the caterpillars are early, then the chicks hatch after the caterpillar numbers have peaked and are on the wane, so that food is less abundant.

The chronology of the tits in the Arnhem forests has not matched the changes in their prey. Temperature largely determines their egg-laying, and to some extent the birds are able to adjust the timing of their reproduction to changing conditions. (They tend to lay earlier in a warm spring.) But their reproduction is complex and involves more than just egg-laying. The birds forage predominantly within larch and birch trees during the egg-laying period, eating insects, spiders and buds, but forage on oaks while rearing chicks. The timing of the larch and birch bud burst has not advanced as fast as it has in the oak, so the different food resources needed during the stages of producing and rearing young have fallen out of sync.

In short, the timing of reproduction in the great tits at Arnhem has not advanced in step with earlier peak availability of food for the young over a 23-year period. This mistiming means that even if the animals can respond quickly, climatic change may not always act uniformly on all parts of the breeding cycle, and constraints and cues may not alter in step with selection pressures acting later in the breeding season. If something happens that upsets that timing — as has been the case in the oak forests of Arnhem — then linkages are broken and whole webs may collapse. Great tit numbers in these forests are in fact in decline, but the implications of climate change are even clearer for long-distance migrants.

Pied flycatchers, for instance, also raise their chicks in the forests around Arnhem and feed them on winter moth caterpillars. They spend the winter in dry tropical forests in West Africa, about 10° north of the equator, and breed in temperate forests in Europe. Although temperatures at the time of arrival and the start of breeding by pied flycatchers have increased significantly in the past decades, the birds have not advanced the spring arrival on their breeding grounds. They have, though, advanced their mean laying date after arrival by 10 days.

Many migrant birds time their departures by effectively using the interaction of their circadian systems and the light signal of the photoperiod, or daylength. It is a complicated process that was first suggested by a German scientist, Erwin Bunning, more than 70 years ago. Knowing the photoperiod (daylength) provides the bird with a calendar, and so it can anticipate the changing of the seasons. In a manner of speaking, it knows the time of year. Many plants and animals also use the photoperiod to synchronize their life cycle to the time of year: when to flower, when to reproduce, when to migrate or hibernate.

But 10° north of the equator the photoperiod is pretty much 12 hours light, 12 hours dark throughout the year, so it cannot use change in daylength for its calendar. Instead, it uses another timing mechanism, an internal circannual clock with a period of about a year that is “fine-tuned” to daylength by the circadian system. We know that there is a circannual clock, but we have very little idea what it looks like, how it works and even where it is in the animal (though it is probably in the brain).

Despite the rise in spring temperatures around Arnhem, the pied flycatchers still leave West Africa the same time of year they always have. Even though they have shortened the time between arrival and egg-laying, a significant part of the population is now laying too late to exploit the caterpillar peak. The “decision” on when to start spring migration has become maladaptive, as the cue used for migration, which is independent of the environmental change in the breeding area, falls out of sync. In areas where the springtime food peaks earlier, the pied flycatcher population has declined by 90 percent. Other long-distance migratory birds could suffer similar declines.

Timing mismatch will have a substantial effect on the survival of many species. Small animals with short life cycles and large population sizes will probably adapt to longer growing seasons and be able to persist; however, many large animals with longer life cycles and smaller population sizes will experience a decline in numbers, or even be replaced in the northern hemisphere by more southern species.

Those organisms that succeed will be the ones with the flexibility to change and adapt to the new temporal regime faster than the speed of the changes in seasonal timing. Some species may migrate poleward. Others may move to higher altitudes. But complete communities will not simply move north or south in synchrony with changing temperatures.

Instead, the blend of plants and animals will change. Climate change could create ecosystems that are unknown today. We do not know what plants and animals they will contain. We do not know what will result when the temporal webs that connect plants and animals are broken. It may be that generations to come will see nature’s wonders. But it is more likely that much of the awe and wonder that obtain from the diversity of life on earth that we know at present will be lost.



See these papers for timing mismatch:

Visser, M. E., van Noordwijk, A. J., Tinbergen, J. M. & Lessells, C. M.(1998) “Warmer springs lead to mistimed reproduction in great tits (Parus major).” Proc R Soc B, 265, 1867–70.

Visser, M. E. & Holleman, L. J. (2001) “Warmer springs disrupt the synchrony of oak and winter moth phenology.” Proc R Soc B, 268, 289–94.

Both, C. & Visser, M. E. (2001) “Adjustment to climate change is constrained by arrival date in a long-distance migrant bird.” Nature, 411, 296–98.

Van Asch, M. and Visser M. E. “Phenology of Forest Caterpillars and Their Host Trees: The Importance of Synchrony” Ann Rev Entomol 2007 57: 37-55

Eberhard Gwinner discovered the circannual clock in birds Gwinner, E. (1989) Photoperiod as a modifying and limiting factor in the expression of avian circannual rhythms. J Biol Rhythms, 4, 237–50.

For the effects of climate change on the survival of species see
Bradshaw, W. E. & Holzapfel, C. M. (2006) “Climate change. Evolutionary response to rapid climate change.” Science, 312, 1477–78.

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Leon Kreitzman has spent much of his working life studying social issues, particularly in health care and aging. His first book, “The 24 Hour Society” (1998), detailed how the new temporal structures are changing the way we live.

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