Animals move to search for resources (e.g. prey, mate, refuge) and to escape stress sources (e.g. predator, inter-species competition). Because the distribution of these external factors and/or animals' internal conditions can change heterogeneously in time, timing of movements is essential for efficient use of the resources and for avoidance of unfavorable situations. In the past, timing of movements between fixed two sites, such as seasonal migration between breeding and overwintering areas, has been well studied in relation of environmental changes with circadian, circannual, and tidal rhythms. However, timing behaviors in more variable situations have little investigated. It is partly because, if sites of departures and arrivals are not fixed and range beyond our observable area, recording of timing of the movements is almost impossible. Recently, miniaturized animal-borne data loggers enable us to obtain fine-scale movement paths of free-ranging animals remotely and continuously. This method should be useful to investigate flexible movements in the wild.

Seabirds perform central place foraging, which is defined as a set of departure from a place ('central place'; e.g. nest and roost), foraging at distant sites, and return to the same place again. Because distribution of their prey at sea is often dynamic, seabirds' movements to search for the prey and the consequent foraging sites are also variable. The need to return may constrain their behavioral range and trip duration, but more than that, the central place could have significance, for example, as breeding and resting sites. Under the presence of the trade-off, decision on when to return the central place appears important in the coordination of their trips. In this thesis, using fine-scale movement paths of seabirds recorded by animal-borne loggers, when to start returning is investigated in two different kinds of central place foraging: diving under the water and flying over the sea. As model species, diving emperor penguins Aptenodytes forsteri and flying streaked shearwaters Calonectris leucomelas are selected.

Emperor penguins: model species of diving seabirds

Emperor penguins are the largest species in the family Spheniscidae. They breed in austral winter on the fast sea ice around Antarctic continent and perform foraging trips at sea. During the trips, they repeat dives not only for foraging but also for horizontal travelling. Emperor penguins have the greatest diving ability among the avian group, of which the deepest record of dive depth was 565 m, and the longest dive duration was 27.6 min.

At some point in a dive, breath-hold divers must decide to return to the surface to breathe. The water surface can be considered as a central place for divers. Longer stay underwater could provide more prey or increase distance traveled, but might also require longer recovery times at the surface as well. In this context, the issue of when to end a dive has been discussed intensively in terms of foraging ecology and diving physiology, using dive duration as a temporal parameter. Inevitably, however, a time lag necessarily exists between the decision of animals to start returning to the surface and the end of the dive, especially in deep dives. Therefore, we examined not dive duration but the decision time to return in emperor penguins by analyzing three-dimensional dive paths. So far, no study has reconstructed fine-scale 3-D dive paths of avian species. Experiments were conducted under two different conditions: during foraging trips at sea and during dives in semi-captive conditions, where penguins dived through an artificial ice hole in an enclosure. It was found that there was an upper limit for the decision-to-return time irrespective of dive depth in birds diving at sea. However, in a large proportion of dives performed by the semi-captive birds, the decision-to-return time exceeded the upper limit at sea. This difference between the decision times in the two conditions was accounted for by a difference in stroke rate. The stroke rates, which were counted from acceleration data, were much lower in dives in the semi-captive conditions and were inversely correlated with the upper limit of decision times in individual birds. Unlike the decision time to start returning, the cumulative number of strokes at the decision time fell within a similar range in the two experiments. This finding suggests that the number of strokes, but not elapsed time, constrained the decision of emperor penguins to return to the surface. While the decision to return and to end a dive may be determined by a variety of ecological, behavioral and physiological factors, the upper limit to that decision time may be related to cumulative muscle workload.

Streaked shearwaters: model species of flying seabirds

Streaked shearwaters are pelagic seabirds in the family Procellariidae. They breed in east and Southeast Asia, mainly in Japan and Korea, nesting underground at islands. During chick-rearing period, they repeatedly commute to the sea for foraging and return to the island to feed their chick as typical central place foragers.

In the foraging trips of some seabird species including streaked shearwaters, while foraging areas disperse widely up to several hundred kilometers from the nesting colony, arrival times at their colonies concentrate within several hours after sunset. This temporal pattern raises the question of how they manage to time arrivals over largely variable homeward distances. However, no study has investigated their at-sea behavioral patterns associated with arrival times. To explore this question, we tracked breeding streaked shearwaters with GPS data loggers, which continuously recorded fine-scale movement paths during their trips. Their foraging areas in long trips varied from 96 km to 457 km in the distance from their colonies. Shearwaters adjusted the onset of their homeward journeys according to the wide-ranging distances between their chosen foraging areas and breeding colonies, leaving earlier from further locations. In the farthest trip, the bird left early in the morning, while in the nearest one, homing started a few hours before sunset. The start time of homing was pushed forward correlating with the increased travel time expected from their homeward distance and average movement speed. This resulted in arrivals at the colony concentrated within a few hours after sunset independent of the distances. To our knowledge, similar temporal tuning of homing trips has not been reported previously in non-human animals. The strong correlation between the timing and distance of homeward journeys implies the compromise between the demand for foraging at sea and the need to arrive at the colony within a specific time window. Their night arrival has been ascribed to the presence of diurnal predators such as raptors, and a previous study on a related species, Manx shearwaters, suggested that the concentration of arrivals after sunset reflect navigational mechanisms depending on diurnal cues such as sun. Thus, streaked shearwaters appeared to time homing trips to overcome several constraints at the same time.

Comparative discussion

Both of the two species did not change moving speeds depending on the distances to their central places: in emperor penguins, mean swim speeds to the surface distributed around 2.1 m s(-1), and in streaked shearwaters, around 9.6 m s(-1). Biomechanical models predict that cost of traveling (J m(-1)) in fluid depends on moving speed and that the speed minimizing the cost is independent of traveled distances. The empirical ranges of moving speeds were consistent with the cost-minimizing speeds estimated by the model. Thus, moving speeds appeared to be constrained by cost efficiency.

As the onset time and speeds of movements are the main determinant of arrival times, given that speeds should not be changed, the importance of the timing to start returning would become increasingly evident. The fine-scale movement paths of diving emperor penguins and flying streaked shearwaters indicated that there were some tendencies in the timing of the decision to start returning. In the penguins, the upper limit of the time to start returning was related to muscle workload, i.e. a physiological factor. This seems reasonable for breath-holding divers because deciding too late at depth would lead directly to death. In the shearwaters, on the other hand, the onset of homeward trips was adjusted according to changes of travel time expected from their flight performance. This could be an adaptation to the combination of dynamic prey distribution and the constraint on arrival times. The timing of the decision to return in shearwaters was likely to relate to the predator avoidance and navigational mechanism, i.e. ecological and cognitive factors. Comparison of the two seabird species under the different situations revealed that timing to start returning could be affected by several kinds of constraints. Considering they travelled in natural environments, where many potential factors may affect their movements, the decision rules found under such complicated conditions should have a great significance for their survival. Novel analyses of fine-scale movement data indicated that seabirds timed their inward movements according to variable situations and that timing ability for the onset to return is the key to solve the trade-off in central place foraging.

動物は餌などの資源を探索したり、捕食者や種内競争を回避する事を目的に移動する。餌分布などの外的要因や動物自身の生理状態といった内的状態は時間と供に変化する。したがって、移動のタイミングは動物の生存や繁殖にとって重要な意味を持つ。繁殖地と越冬場所など、決まった二点間を季節移動したり、日周リズムや潮汐変化などに対応した動物の定期的な移動については数多くの先行研究例がある。しかし、毎回移動距離が異なるという動的な状況下で、動物がいかにして移動のタイミングを決定しているのかについては、これまでほとんど調べられてこなかった。その理由としては、人間が直接観察できない水中の移動や、数百kmを超える広範囲な水平移動を測定する手段が無かったことが挙げられる。本研究では、近年開発された動物搭載型記録計を用いて、海鳥類が水中や空中を移動する際の経路を測定し、海鳥類の移動のタイミングが何によって左右されているのかという点に着目して解析している。

最初のモデル種として、南極海の定着氷下で潜水を繰り返すエンペラーペンギンを選んだ。エンペラーペンギンは、餌生物の分布深度に応じて、深度10m程度の浅い潜水から最大500m以上の深い潜水を行う事が知られている。また、深度が浅い潜水であっても水平方向に1km以上移動した後に、再び潜水開始点まで引き返す場合がある事が判明した。肺呼吸動物であるペンギンは、体内に蓄積した酸素を使い果たすまでに必ず水面に戻らなければならない。鉛直的にも水平的にも広い移動範囲を持つエンペラーペンギンが、生理的限界時間に達する前に潜水を終了させるためには、水面に向かって引き返し始める決断をいつ下すかが重要である。そこで、地磁気・加速度・遊泳速度・深度から算出される水中三次元遊泳経路より、ペンギンが水面に向かって引き返し始める点を抽出したところ、潜水開始からの経過時間ではなく、フリッパーを動かした回数によって、引き返しを決断する時間の上限が決まっている事が判明した。フリッパーを打ち振る回数は、筋肉の仕事、すなわち酸素消費量に比例すると考えられ、ペンギンは筋肉の酸素消費量が一定値に達した時点で引き返しを決断するといった、応答的決断を行っていたものと解釈された。なお、本研究は世界で初めて潜水性鳥類の水中三次元経路を得たものであり、その計算アルゴリズムの一般化や測定精度の検討なども本研究が本学問分野に対してなした重要な貢献である。

次に、飛翔性鳥類であるオオミズナギドリをモデル種として、水平移動経路分析を実施した。日本列島周辺の島嶼において繁殖を行うオオミズナギドリの雄雌は、育雛期間中に採餌旅行に出かけ、海上で魚類を漁って巣に持ち帰ることを繰り返している。過去になされた観察により、親鳥は日の入り直後に島に戻り、日の出直前に再び採餌旅行に出かけていくことが知られている。本研究で、オオミズナギドリに搭載可能な小型GPSを用いて採餌旅行中の移動経路を調べたところ、島のごく近傍で採餌してその日の内に島に戻ってくる日帰り採餌旅行から、500km以上離れた北海道東岸海域で採餌した後島に戻ってくる1週間程度の長距離採餌旅行まで、長短入り交じった採餌旅行を繰り返し行っている事が判明した。島へ到着する時刻は、餌場と島の距離とは無関係で、日の入り後3時間以内に集中していた。オオミズナギドリがいかにして帰島時刻を調節しているかを調べるために、水平移動経路において餌場から島に向かって戻り始めた時点を抽出し、島からの距離と時刻を比較した。その結果、島から遠く離れるほど、戻り始める時刻が早まる傾向が見つかった。さらに、その回帰直線の傾きは1kmあたり0.036時間(2.16分間)となったが、この値は鳥の平均飛翔速度34.7km/hと帰りに要した時間の内飛翔にあてた時間割合80.9%から計算される1kmあたりの所要時間0.036時間{=1/(34.7x0.809)}に一致した。オオミズナギドリが自らの移動能力や島からの距離に応じて、島に向けて出発する時刻を調節するという予見的決断を行っている事を示唆する結果となった。

対象とした2種のモデル種は、移動の際に2.1m/sないし9.6m/sという速度で遊泳や飛翔をしていた。既存のバイオメカニクスモデルを修正して検討したところ、これらの値はそれぞれの種における移動コストを最小とする速度であった。2種の鳥類において、移動距離に応じて移動速度を変えるのではなく、戻り始めるタイミングの決断が移動に関わる意思決定において大きな役割を果たしている事を指摘した本論文の研究結果は、動物の移動に関わる研究分野において今後進むべき重要な方向性を提示している。よって審査委員一同は、本論文の学術的価値が高く、博士(農学)の学位論文に十分値するものと認めた。