The authors have declared that no competing interests exist.
Erect-crested penguins are the least studied of all penguins. They breed on two isolated subantarctic island groups, the Antipodes and Bounty Islands. Sporadic nest counts indicate a dramatic decline in numbers of erect-crested penguins over the last 50 years. Here we present data from a study undertaken in 1998 on the breeding biology, behavior and hormones of erect-crested penguins. It represents, even today, by far the most detailed data available on this species. The penguins exhibited extreme reversed egg-size dimorphism, whereby the first-laid A-egg was much smaller than the second-laid B-egg. A-eggs were lost before (42.3%) or on (37.8%) the day the B-egg was laid, and none survived more than 7 days after that. The penguins were in a low state of reproductive readiness, as evidenced by low levels of copulation, fighting, and testosterone in males during the courtship/laying period when, curiously, plasma levels of testosterone were at least as high in females. The laying interval (5.4 days) is the longest recorded for any penguin species, and incubation was highly variable until clutch completion. Most nests (91.2%) contained no nesting material and eggs were laid directly onto the ground. A-eggs were lost mainly by rolling out of the nest. However, even when prevented from doing so by an experimental manipulation, A-eggs survived no longer than those in control nests. Testosterone levels in males increased after clutch completion, when they remained in attendance at the nest for up to 13 days, despite females assuming most of the incubation duties. The bills of males were significantly larger than those of females and probably help with guarding the nest. We discuss explanations for obligate brood reduction in crested penguins and the options for conservation in light of our census results, which indicate that this enigmatic penguin species could be in trouble.
When three of us (LSD, MR and DH) went to the Antipodes Islands in 1998 to conduct research on the erect-crested penguin (
The erect-crested penguin belongs to the genus
Erect-crested penguins breed mainly on the Antipodes and Bounty Islands from September to late January and remain offshore between breeding seasons [
There have never been any full-season observations at the breeding colonies of erect-crested penguins. Systematic research on this species is very limited. Richdale [
Birds often face limited amounts of available natural resources, especially with regard to the availability and distribution of food. In particular, when breeding, parent birds must acquire enough food to meet the energy requirements for breeding while also allocating sufficient resources to their chicks [
Christians [
The most extreme variation in egg size of all birds is reported in the crested penguins [
Researchers have paid increasing attention to such an enigmatic trait of
An early hypothesis to explain the function of the smaller egg suggested that it may be an insurance against the possible loss of an egg [
Another hypothesis suggested that the A-egg may provide stimulation for forming the brood patch [
Another hypothesis is that the small A-egg does not have a specific adaptive function but its size is a consequence of a physiological constraint (the migratory carry-over effect) [
In summary, up till now, there has not been a widely accepted hypothesis for the egg-size dimorphism and obligatory brood reduction of crested penguins due to a lack of systematic data and relevant experimental tests in breeding colonies of different species of crested penguins, particularly those with extreme egg-size dimorphism [
In this paper, we present data from a study of erect-crested penguins carried out on the main Antipodes Island from 18 September to 2 November 1998, which covered the courtship and laying periods. We conducted a census of a subsample of colonies breeding on the island, and followed the fates of 270 banded individuals in a single study colony using 113 nest sites. We measured the degree of sexual dimorphism of males and females, recorded the dates of laying, plus the timing and causes of egg losses. Using penguins breeding in another colony, we sampled the degree of egg-size dimorphism, took blood samples to measure levels of testosterone and estrogens, and conducted an experiment to reduce losses of A-eggs by preventing them rolling away from the nest. Our aim here is to present information on the breeding biology of erect-crested penguins that may be used to foster understanding of the causes for their population declines and the reversed egg-size dimorphism and obligatory brood reduction characteristic of these penguins.
We studied erect-crested penguins breeding on Antipodes Island, which is the largest island of the Antipodes Islands archipelago some 860 kilometers south east of New Zealand, from 18 September– 2 November 1998.
The main study colony (hereafter termed, Study Colony) was atop a relatively flat rocky platform in Anchorage Bay (49°39’57”S, 178°47’59”E). It was chosen because all nests in the colony could be observed simultaneously from an observation platform on the adjacent cliff face.
Before any egg-laying began in the Study Colony, 270 erect-crested penguins were caught by placing a net on a long pole over them. They were flipper banded, weighed with a Persola balance (±5g), and morphometric measurements were taken of their bill length, bill depth, flipper length, foot length and crest length using calipers (± 0.05mm). The birds had a unique code of a letter and a number painted on their backs in yellow enamel paint so that they were individually identifiable from the observation platform. Thereafter, the Study Colony birds were not handled again in any way and the colony was not entered again by us.
We observed the Study Colony for up to 12 hours/day, for a total of 249 observation hours, from 29 September to 22 October. This coincided with the courtship, laying and immediate post-laying periods. We used all-occurrences sampling [
Sizes of 22 A-eggs were measured using calipers (± 0.05mm) and weighed (±0.25g) from a sample of nests in the Study Colony when the A-egg had been rolled out of the nest and we were able to collect the egg without entering the colony or displacing the nesting birds. Laying dates were known for 16 of the eggs. Sizes of 51 B-eggs were measured similarly at the conclusion of the study, of which the laying date was known for 49. A pole was used to gently leverage the rear end of the bird so the B-egg could be removed and measured quickly. The whole procedure took about a minute and, when the egg was replaced in the nest, all birds resumed incubation.
Discriminant function analysis (DFA) is a statistical technique used to make decisions about naturally occurring group membership, such as sex. It is a commonly used method used to sex penguins, which are monomorphic in appearance, whereby a function combining morphometric measurements such as bill length, bill depth, flipper length or foot length is determined that best predicts the sex of a bird accurately [
A sample of 42 nests of erect-crested penguins breeding in a nearby colony, also in Anchorage Bay, was used for an experimental manipulation. A ring of stones was placed around 14 nests (Experimental Group) to prevent eggs being rolled away from the vicinity of the nests to determine whether this could influence retention and survival of the first-laid A-egg. There were 28 nearby nests in the colony were monitored as a Control Group. The 42 nests were inspected daily to record the dates that A-eggs and B-eggs were laid. A chinagraph pencil was used to mark the A- and B-eggs for identification. The dates of egg losses, fates of lost eggs, and the date that the female began the first incubation spell (i.e., the date on which the male had departed for sea) were recorded.
Blood samples (1ml) were taken from the brachial vein of penguins breeding in nests elsewhere in Anchorage Bay during egg-laying (n = 5 males; 5 females), the post-laying guard period (n = 6 males; 6 females), and the first incubation spell (n = 6 females). Following that, morphometric measurements of the penguins (bill depth, bill length) were taken, as described above, which were used in combination with behavioral observations to determine their sex. Measurements and blood sampling were completed within 5 minutes for each bird. Individual birds were sampled only once.
Plasma was separated from blood by centrifugation within 1 hour of bleeding and immediately frozen by storing in liquid nitrogen. Upon return from the Antipodes, samples were kept at -80°C until analyzed within the next 12 months. Plasma concentrations of the sex steroids estradiol and testosterone were measured by specific radio-immunoassays. The sex steroids were extracted in diethyl ether and assayed using the methods of [
On 27 and 28 October, we carried out a census of erect-crested penguins breeding at five locations on Antipodes Island (Alert Bay North, Orde Lees, Anchorage Bay, Stella Bay and Reef Point). The locations were suggested by the Department of Conservation in order to be comparable with previous counts made on Antipodes Island. Three of us (LSD, MR, DH) each counted the number of active nests of breeding birds using hand counters and the counts were averaged. Orde Lees was difficult to count accurately due to the large number of birds present and our limited access, which meant that the penguins had to be counted from a distance of over 100 meters using binoculars. As an alternative to using the hand counters, each of us also counted the number of sections containing 70 birds that fit within the colony.
Data were analyzed using MS Excel and SPSS Version 24.0. Permits for landing on Antipodes Island and handling the erect-crested penguins were issued by New Zealand’s Department of Conservation (permit #s 98-99/443/01/07, 98-99/443/10/03, and 98-99/443/05/01).
In all, we banded 270 individual penguins in the Study Colony from 20 September to 30 September, which included 136 males, 121 females and 13 for which we did not have any corroborating evidence to assign a sex. The sex of individual penguins was verified by either observation of copulatory position, tread marks on the back (indicating a female), performance of ecstatic displays during the courtship period (indicating a male), or a combination of these. Males and females were sexually dimorphic, with male penguins being significantly larger than females in all morphometric measurements except crest length (
Females (n = 121) | Males (n = 136) | |
---|---|---|
Weight (kg) |
5.11 ± 0.35 | 5.24 ± 0.35 |
Bill length (mm) |
54.68 ± 2.08 | 60.05 ± 2.30 |
Bill depth (mm) |
22.66 ± 0.89 | 26.14 ± 1.10 |
Foot length (mm) |
118.68 ± 3.71 | 123.92 ± 3.47 |
Flipper (mm) |
163.88 ± 4.15 | 171.15 ± 5.11 |
Crest (mm) | 53.04 ± 3.24 | 52.94 ± 3.44 |
Measurements are given with standard deviations (SD).
** indicates a significant difference between females and males (
Discriminant function analysis (DFA) showed that using bill depth and bill length allowed assignment of sex with 96.9% accuracy in the Study Colony. The discriminant function indicates that bill depth is the most important variable to discriminate between sexes (Wilks’ Lambda = 0.250, F = 764.700, P < 0.001), followed by the bill length (Wilks’ Lambda = 0.400, F = 382.181, P < 0.001; NB: a smaller value of Wilks’ Lambda represents a better predictor). Calculating a Bill Index by multiplying bill depth (mm) × bill length (mm) proved to be the best predictor in the discriminant model for assigning sex in erect-crested penguins (Wilks’ Lambda = 0.231, F = 846.875, P < 0.001, overall accuracy = 96.9%). As a simple rule, sex can be assigned with reasonable confidence if the Bill Index is under 1331.0 (probability of female = 95.0%) or over 1478.5 (probability of male = 95.0%). Using just this simple rule accurately identifies the sex of 86.3% of the birds in our Study Colony, with only 13.7% of birds falling within the overlap range.
The majority of the 158 penguins present in the Study Colony when we began our observations and banding on 20 September were males. Of the 24 birds that we caught and banded that day, 19 (79.2%) were males and only 5 (20.8%) were females. If that ratio was a representative sample, then the colony would have contained around 125 males at the start of this study. Thereafter, numbers of birds in the colony increased steadily, especially due to an influx of females, reaching 290 by 2 October and staying at 290 ± 3 until 16 October (
The nests of the erect-crested penguins were extremely simple: of 113 nests in the Study Colony, 103 (91.2%) did not use any nesting material at all, with the birds laying their eggs on the rocks or bare ground. Only 10 (8.8%) nests contained any nesting material and this consisted mostly of straw-like dried grasses.
During the courtship period, males lost body mass at a significantly greater rate (63.8g/day) than did females (53.6g/day) (P<0.05). Males also tended (P = 0.06) to spend a higher percentage of their time fighting (0.25%) than did females (0.05%) during the courtship period, although in both sexes the amount of fighting was very low and fights were infrequently observed in the Study Colony. Copulation rates were also very low, with a mean of 0.03 copulation attempts per hour per pair.
The first A-egg was laid in the Study Colony on 3 October and the last clutch was initiated on 14 October. The mean date for laying A-eggs was 8 October (SD = 2.42, n = 118) and the mean laying date for B-eggs was 13 October (SD = 2.57, n = 112). The mean intra-clutch laying interval was 5.38 days (SD = 0.96, n = 111) with the range being 4–9 days. For 93.6% of nests the laying interval was 4–6 days (
Of the 111 A-eggs from two-egg clutches, none survived more than a week after the B-egg was laid, with the vast majority (80.1%) being lost before (42.3%) or on the day of the B-egg being laid (37.8%) (
Of A-eggs monitored in 113 nests in the Study Colony, only about a quarter (24.8%) were lost within the nest, either through the parents ignoring the egg and not incubating it (14.2%) or breaking it (10.6%) (
For 29.2% of nests, the A-egg was observed outside the vicinity of the nest, while for another 26.5% of nests the A-egg disappeared from one observation period to the next, most likely from rolling off the slightly sloping rocky platform on which the colony was sited or being taken by skuas once the egg was outside the nest. We observed two means by which the eggs ended up out of the nest: in 13 nests (11.1%), the A-egg was observed being rolled from the nest, seemingly accidentally, as a consequence of the incubating parent shuffling about on the nest while trying to adjust the eggs against its brood patch. This occurred especially on the day the B-egg was laid, as the birds tried to accommodate both the large B-egg and much smaller A-egg. In 7 instances (6.2%), we observed a parent bird peck at the A-egg, rolling it away from the nest. Fights were remarkably rare compared to other penguins during the courtship and laying period (see below), and in only 2 instances (1.8%) were A-eggs broken as a consequence of fighting in the colony (
Correlations of the age at which the A-egg was lost with body mass of the female and the dates of laying the A- and B-eggs are presented in
Significant correlations are shown with bold lines (** P < 0.001; * P < 0.05).
The intra-clutch egg size dimorphism was extreme (
A-egg | B-egg | |
---|---|---|
Length (mm)** | 69.17 ± 3.75 | 83.84 ± 3.28 |
Breadth (mm)** | 46.41 ± 1.68 | 57.55 ± 2.05 |
Volume (mm3)** | 77987.73 ± 7870.17 | 139631.44 ± 12651.83 |
Mass |
81.55 ± 7.56 | 150.94 ± 17.92 |
The volume was calculated based on length and breadth, according to Narushin [
1Mass was available for n = 20 A-eggs.
There is the suggestion of a tendency for the mass of A-eggs to increase with laying date (Pearson’s
Instantaneous scan sampling revealed that between the laying of the A-egg and B-egg, 40% of pairs largely neglected the A-egg and did very little incubation (
** indicates that the difference between males and females is highly significant (P < 0.01).
A ring of stones was added around 14 nests in the Experimental Group in order to test whether the longevity of the A-egg could be increased if the A-egg was prevented from being rolled away from the nest either accidentally or deliberately. The Control Group consisted of 28 unmanipulated nests. The ring of stones significantly promoted retention of A-eggs in the nest, with 86% of A-eggs in the Experimental Group being retained in the nest compared to only 4% in the Control Group (
In the Experimental Group, 64.3% of the A-eggs were broken in the nest, while 21.4% were not incubated even though retained in the nest. By contrast, in the Control Group, the A-egg was found rolled away from the vicinity of 55.2% of nests and had disappeared from a further 34.5% of nests (
As expected, plasma levels of estrogens were significantly higher in females during laying compared to males (
* indicates that the difference between estrogen levels in males and females is significant (P < 0.05).
By contrast, plasma levels of testosterone did not follow expected patterns. During laying, mean testosterone levels were actually higher in females than males, though the variability amongst females was high and, given the small sample sizes, the apparent difference proved not to be significant (
This coincided with the period when the male stays at the nest with the female post-laying. The duration the male stays at the nest post-laying was highly negatively correlated (Pearson’s
The total number of erect-crested penguins counted by us on 27–28 October 1998 at five locations on Antipodes Island was 7,510. Compared with a census at the same locations in 1995 [
Location | Mean | Standard error | 1995 counts | Change |
---|---|---|---|---|
Alert Bay North | 324 | 7 | 421 | -22.96% |
Orde Lees |
4582 (6627) | 228 (639) | 8720 | -47.45% (-24.00%) |
Anchorage Bay | 1646 | 18 | 2779 | -40.77% |
Stella Bay | 303 | 3 | 330 | -8.08% |
Reef Point | 654 | 11 | 713 | -8.27% |
Means (±se) are calculated from the counts of three different observers on the same day.
*Numbers of birds breeding at Orde Lees were also estimated by counting the number of blocks of 70 nesting penguins that fit within the observed area of nesting birds. This count is shown in brackets. Comparisons between the 1998 and 1995 counts [
The accuracy of our counts at Anchorage Bay, Stella Bay and Reef Point was very high. These three locations were also censused in 2011 [
Location | 1995 | 1998 | 2011 | 2014 | Change (%) |
---|---|---|---|---|---|
Anchorage Bay | 2779 | 1646 | 2048 | 1673 | -39.8 |
Stella Bay | 330 | 303 | 251 | 222 | -32.7 |
Reef Point | 713 | 654 | 578 | 505 | -29.2 |
Compared to other penguin species, indeed other species of the genus
Royal penguins have been observed to deliberately eject the A-gg [
Approximately half of the pairs do little to no incubation of the A-egg prior to laying of the B-egg. Together with very low copulation rates, which are an order of magnitude less than comparably-sized Adelie penguins [
The hormonal levels would seem to support this, with testosterone levels in males being unexpectedly low and in females being unexpectedly high during the laying period. The increase in testosterone in males during the post-laying period when, unlike non-crested penguins, the male remains at the nest with the female after laying, could well be associated with males defending incubating females from “bullying” behavior [
Our results are not consistent with two of the main hypotheses regarding the reversed egg size dimorphism and obligate brood reduction. First, very few A-eggs are lost to fighting during the courtship period and fighting occurs at very low levels, making it unlikely, as suggested by Johnson et al. [
As Davis and Renner [
The high levels of testosterone we found in females during the laying period may help explain the mechanism for reducing investment. Erect-crested penguins are migratory [
In sum, the migratory carry-over effect may well explain the mechanism for why crested penguins should invest in the B-egg preferentially as vitellogenesis, which begins in migratory penguins while they are still travelling at sea [
Just as unclear as the evolutionary purpose of the erect-crested penguin’s brood-reduction strategy are its population developments in the past decades. The IUCN red list currently ranks erect-crested penguins as “endangered” due to substantial discrepancy in penguin numbers determined in the late 1970s and counts conducted since the mid-1990s [
On the Bounty Islands, penguin numbers until recently were believed to have dropped by more than 75% since 1978 [
There is similar uncertainty in population estimates of erect-crested penguins on the Antipodes Islands between the late 1970s and the 1990s. Taylor [
These discrepancies highlight the problem with largely opportunistic monitoring of species that are limited to remote locations. More often than not penguin counts are tacked onto expeditions that focus on other conservation or scientific goals and occur sporadically, with large temporal gaps in between subsequent surveys reducing the available data to little more than a series of snapshots that make it difficult to draw any robust conclusions about population trajectories. This is further compounded by the surveys on erect-crested penguins being primarily conducted by New Zealand’s Department of Conservation, which is severely limited in its resources available to carry out this work [
Nevertheless, it seems likely that climate change is negatively impacting erect-crested penguins breeding on the Antipodes Islands. Increased storm frequencies over the past decades likely contributed to an increased occurrence of landslips, especially in the south of Antipodes Island, which wiped out parts of colonies and killed penguins attending their nests [
However, unless erect-crested penguins receive the scientific attention their current red list ranking demands, the species will remain the enigma of the penguin family.
Remaining an enigma will not change the plight of erect-crested penguins. Research priorities increasingly determine prospects for survival of many species around the world [
We thank Graham Young and Shirley McQueen for assistance with the hormonal assays.