1.1 Retrospective Mortality Studies in Zoos

Retrospective studies of zoo mortality have great potential in identifying methods of improving animal management (Hanselmann et al. 2013; Thorel et al. 2020; Trumpp et al. 2021). Mortality case studies can be useful, but the disease found in one individual is not reflective of an entire population. When viewed from an epidemiological level, trends in population mortality and lifespan can be identified (McCreesh et al. 2023). For example, recent population-level research identified limited evidence of senescence in captive testudines (da Silva et al. 2022). Retrospective zoo mortality studies have been completed for a range of taxa including primates (Glatston 2001; Strong et al. 2016), big cats (Duque-Correa et al. 2022; Thorel et al. 2020), and a range of bird species (Krol et al. 2020; Lamglait 2018; O'connor et al. 2022; Reed, Anderson, and Wolf 2021; Shopland et al. 2020; Trumpp et al. 2021). While there are occasional case studies of secretarybird mortality (Wack, Kramer, and Anderson 1994), there are no retrospective mortality studies available.

One of the problems for the captive secretarybird population is high mortality in comparison to wild birds (Kemp 1995). Secretarybirds have a slow life history, with a generation length of 9.3 years (IUCN 2020). Breeding is irregular and chicks are not produced every year (Kemp 1995). As recruitment of offspring is gradual, low adult mortality is central to the sustainability of secretarybird populations.

Investigation of the causes of death of EEP-managed secretarybirds has useful applications for population management. By identifying common causes of death, animal managers can adjust their management protocol to reduce mortality, and therefore increase individual lifespan. This may in turn provide opportunities for increased breeding, as birds live through a greater number of breeding seasons. This study therefore aimed to identify common causes of death in secretarybirds in the EEP population.

2.1 Data Analysis

Data were collated using Microsoft Excel, and analysis was undertaken using Minitab, version 21 (Alin 2010). An α value of 0.05 was set for all statistical analysis. Average age at death and cause of death were identified using the average for each sex and age group. Chi-squared tests were used to test whether there was a significant difference in mortality between life stages and sex. Secondary circumstances were tested using binary logistic regression to determine whether age and sex were predictors of death, using the additional records of living secretarybirds and using dead or alive as the binary variable. To carry out binary logistic regression, individuals missing data on sex, age, or information pertaining secondary circumstances were not tested.

Additional graphs were developed using the zoo population management software, PMx (Lacy, Ballou, and Pollak 2012), using data extracted from the ZIMS for studbooks data for the secretarybird. These graphs were used to demonstrate population longevity, and also demographic reproductive success for the species, based on current ZIMS records.

3.1 Number of Mortality Events

A total of 167 secretarybirds were identified were identified as dead in the EEP population. This consisted of 55 (32.93%) female, 67 (40.12%) male, and 45 (26.95%) unidentified birds. Of these deaths, information was available on the cause of death for 51 (30.54%) birds from 14 different institutions.

3.2 Cause of Death

The cause of death for secretarybirds was separated by sex. Overall, the most common known cause of death was trauma (N = 22, 13.17%), followed by infectious disease (N = 15, 8.98%) and neonate mortality (N = 4, 2.40%) (Table 3). A total of four birds (2.40%) were euthanized; the reason for the euthanasia is reported as the cause of death.

One secondary finding identified at postmortem was liver damage for 9 (5.39% of birds). However, as liver damage could only be identified by postmortem, the prevalence of damage is potentially quite high (9 out of 51 birds with PMRs, 17.64%). Liver damage included bacterial hepatitis, staphylococcal infection, lesions, and darkened color indicative of hemochromatosis. Arthritis was identified as a secondary finding in two birds (0.60%) and atherosclerosis occurred in a further two birds (0.60%).

3.3 Life Stage

Secretarybirds were categorized by life stage, based on their time of death (Table 4). The majority of birds died as adults (43 birds, 25.75%), followed by geriatric individuals (45 birds, 26.95%). However, it should be noted that the adult and geriatric periods were the longest life stages, with chick (3 months) and juvenile (45 months) lasting comparatively shorter periods. Trauma was the most common cause of death in both adult and geriatric birds, whereas neonate mortality was most common for chicks, and infection was the most common cause of death in juveniles. The longevity of birds was plotted descriptively (Figure 1). The binary logistic regression identified no significant predictors of mortality (χ²₍₁₇₄₎ = 136.73, p = 0.976), with the model explaining only 5.15% of variance. A figure of reproductive success (Mx) for captive birds in the EEP is also provided (Figure 2).

3.4 Sex

Secretarybird mortality was broken down by sex and age (Table 5). There was a nonsignificant difference mortality between males and females in terms of life stage (χ² = 6.816, p = 0.078).

4.1 Cause of Death

Trauma was the most common cause of death for secretarybirds. Trauma was caused by a myriad of events, including aggression with conspecifics during introductions, interactions in mixed-species enclosures, and damage caused by collisions with exhibit furnishings. Anatomically, secretarybirds are predisposed to trauma, given their long legs and neck (Dick 2017). While intuitively it would appear that keeping secretarybirds as single individuals in exhibits could reduce trauma risk, this may not always be the case. Combination of birds for breeding purposes is still required, and keeping of secretarybirds in large, mixed-species enclosures may have hidden benefits that reduce trauma risk, such as greater exhibit space and therefore lower risk of collision against enclosure barriers (Green, Palmer, and Brereton 2022). Trauma could be reduced by making introductions of pairs of secretarybirds slowly and by providing ample space for movement so as to avoid collisions with exhibit walls and netting, following introduction guidelines such as those used for zoo-housed cranes (Gee 1983).

Infection was the second-most common cause of death in secretarybirds. Infection has been shown to be a common cause of death in zoo animals (Galosi et al. 2015; Gibson et al. 2019; Scaglione et al. 2019; Shivaprasad 2003), with infections affecting a multitude of organ systems. Birds may be especially susceptible to respiratory disease due to their complex air sacs and unidirectional lungs (Gibson et al. 2019). A range of bacteria and viruses were suspected in secretarybirds, but pathogen identification was rarely conducted. A call for more detailed PMRs would aid in identifying the greatest pathogen risks for this species, and this may aid in developing strategies for reducing these risks.

The identification of liver damage on numerous occasions at postmortem is an unexpected finding. In many cases, the liver damage was not the primary cause of death but rather an incidental finding. Livers were described as showing lesions, with the majority being dark in color, with evidence of bacterial hepatitis. Similar findings have been identified in a published case study of a secretarybird postmortem (Wack, Kramer, and Anderson 1994). There may be an association between liver damage and systemic infection. For example, hemosiderosis; the accumulation of iron in the liver, is believed to predispose animals to infection (Leone et al. 2016). Dark liver color is often associated with hemochromatosis; these findings are often identified in rainforest birds such as toucans and mynahs (Galosi et al. 2015; O'connor et al. 2022). Hemosiderosis rarely occurs in carnivorous birds, which have developed mechanisms to reduce iron absorption (de Oliveira et al. 2022). However, it is possible that captive birds receive more available iron in their diet than wild birds.

One other explanation for liver damage could be excess protein. Inappropriate levels of protein and fat can place metabolic pressure on the liver (Díaz-Rúa et al. 2017). While different species have differing requirements for fat and protein, there may be a mismatch between the protein requirements of the natural diet versus the diet fed in captivity (Flacke et al. 2017). While the secretarybird is commonly purported to be a snake-eater (Davies, Retief, and Smit-Robinson 2014; Portugal 2022), invertebrates also play a role in the diet. In captivity, other food items, such as day-old chicks, mice, and rats are often fed (Wennrich 1984), which may be lower in fiber and higher in fat and protein. Further investigations of both the captive and wild diet may have value.

Occasional incidences of arthritis and atherosclerosis were noted at postmortem for secretarybirds. However, both were identified only rarely at postmortem, and as such their incidence is likely to be low. Both tend to be associated with older animals (Beaufrère et al. 2013), so the limited incidence of these findings suggests that birds are not always reaching old age.

4.2 Life Stage

Overall, the two life stages in which the majority of secretarybirds died were as juveniles and as geriatric birds. However, the geriatric period is a much longer period, encompassing any birds over 15.5 years, whereas juvenile birds consisted only of individuals between 3 and 48 months. This demonstrates that the period with the highest chance of mortality for a secretarybird is their first 2 years (see Figure 1). High neonate mortality is common across a range of raptors (Battisti et al. 1998). In the wild, adult secretarybirds live long lives, (Hofmeyr, Symes, and Underhill 2014), and recruitment is low due to small clutch sizes and irregular breeding. As a relatively K-selected bird (with a long lifespan and slow reproduction), low adult mortality is important for population sustainability (Balbontín et al. 2012). It is therefore promising that mortality is not excessive for adult birds. It should be noted, however, that secretarybirds have been shown to breed until at least their 20's (27 for males, 28 for females), and therefore many of the “geriatric” birds may still be reproductively viable (Dick 2017). The upper limit for secretarybird longevity is not yet known; several birds in the EEP are still alive at over 30 years old. The fact that the oldest birds are still alive suggests that there is a trend toward lengthening lifespans in captive secretarybirds, though more data are required to confirm this.

4.3 Sex

There was no significant difference in mortality between male and female birds in terms of life expectancy or causes of death. Both males and females lived a similar amount of time, with both equally likely to die as chicks or juveniles. However, it should be noted that the amount of data on mortality in the studbook is limited (167 birds). Clearer information on sex-specific mortality may become available as the EEP progresses, and more animals are inputted into the data.